Assessment of antimitotic and programmed cell death stimulation potentials of Galium sinaicum (Delile ex Decne) Boiss. at the cellular level
DOI:
https://doi.org/10.36253/caryologia-1057Keywords:
Galium sinaicum, programmed cell death (PDC) hallmarks, Allium cepa, MCF-7, BHK21, HPLCAbstract
Galium sinaicum is a wild medicinal plant in saint Catherine, Egypt. To distinguish apoptotic effect of G. sinaicum ethanol extract (GsEE). The role of GsEE in inducing programmed cell death (PCD) of Allium cepa root meristematic cell(AcR) was examined. Cells was subjected to GsEE in definite concentrations (0.1,0.3, 0.5%) and duration (6, 12h), then PCD induction was assessed. Application of GsEE arrested the mitotic division of AcR with metaphase accumulation. Electron microscopy analysis demonstrated ultrastructural alterations of organelles verifying PCD hallmarks. Protein electrophoresis analysis of AcR revealed a change in protein profile of Allium cepa root, also quantitative analysis showed significant increase in nuclease activity enzymes that stimulated DNA laddering fragmentation. Additionally, cell proliferation of MCF-7 and BHK21 was arrested by GsEE. Apoptotic effect of G. sinaicum may be attributed to the presence of potent phenolic compounds such as querectin and rutin as established by HPLC phenolic fingerprint analysis.
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Amirghofran Z, Bahmani M, Azadmehr A, Javidnia K. 2006b. Anticancer effects of various Iranian native medicinal plants on human tumor cell lines. Neoplasma. 53: 428–433.
Aslantürk ÖS, Çelik TA, Karabey B, Karabey F. 2017. Active phytochemical detecting, antioxidant, cytotoxic, apoptotic activities of ethyl acetate and methanol extracts of Galium aparine L. British J Pharmaceutal Res. 15(6): 1-16.
Avila J, Devarenne TP. 2013. Ubiquitination of the tomato cell suppressor Adi3 by the Ring E3 ubiquitin ligase AdBil. Biochem Bioph Reas Comm. 430: 119-124.
Bao L, Liu F, Guo HB, Li Y, Tan BB, Zhang WX, Peng YH. 2016. Naringenin inhibits proliferation, migration, and invasion as well as induces apoptosis of gastric cancer sgc7901 cell line by downregulation of akt pathway. Tumor Biol. 37: 11365–11374.
Blank A, Mckeon TA. 1989. Single-strand preferring nuclease activity in wheat leaves is increased in senescence and is negatively photoregulated. Proc Nat Aca Sci USA. 86: 3169-3173.
Chen H, Miao Q, Geng M, Liu J, Hu Y, Tian L, Pan J, Yang Y. 2013. Anti-Tumor effect of rutin on human neuroblastoma cell lines through inducing G2/ M cell cycle arrest and promoting apoptosis. The Sci World J. 2013, Article ID 269165, 8 pages.
Cragg GM, Kingston DG, Newman DJ. 2005. Anticancer agents from natural products. Taylor and Francis Group; Brunner Routledge Psychology Press, London.
Domínguez F, Moreno J, Cejudo F. 2004. A Gibberellin-induced nuclease is localized in the nucleus of wheat aleurone cells undergoing programmed cell death. The J Biol Chem. 279 (12): 11530–11536.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation method for small quantities of fresh tissues. Phytoch Bull Bota Society Amm. 19:11–15.
El-Gamal AA, Halim AF, Amer MM, Saad HA, Takeya K, Itokawa H. 1999. Flavonol glycosides from Galium sinaicum. Alex J Pharm Sci. 13 (1): 41-47.
Farr KA, Cohen-Fix O. 1999. The metaphase to anaphase transition. Euro J Biochem. 263:1-14.
Fiskesj? G. 1997. Allium test for screening chemicals; evaluation of cytologic parameters. In: Wang W, Gorsuch JW, Hughes JS. editors. Plants for environmental studies. CRC Lewis Publishers, Boca Raton, New York, pp 308–333.
Fuzinatto VA, Pagliarini MS, Valle CB. 2007. Evidence of programmed cell death during microsporogenesis in an interspecific Brachiaria (Poaceae: Panicoideae: Paniceae) hybrid. Gent Mol Res. 6: 308- 315.
Gao Y, Ma Q, Ma YB, Ding L, Xu XL, Wei DF, Wei L, Zhang JW. 2018. Betulinic acid induces apoptosis and ultrastructural changes in MDA-MB-231 breast cancer cells. Ultrastruct Pathol. 42(1):49-54.
Gîrd C, Costea T, Nencu I, Popescu ML, Du?u LE. 2015. Phytochemical and phytobiological research upon aerial parts and seeds from Peucedanum officinale. Farmacia. 63(2): 247-253.
Gli?ska S, Gabara B. 2000. Localization of selenium deposits in meristematic cells of Allium sativum L. roots treated with selenium salts. Folia Histochem Cytobiol 38:143–147.
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE. 2001. Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta. 212: 205–214.
Güvenalp Z, Kazaz C, Kaya Y, Demirezer LO. 2006a. Phytochemical investigation on Galium humifusum growing in Turkey. Biochem Syst Ecol. 34:894-89.
Güvenalp Z, Kilic N, Kazaz C, Kaya Y, Demirezer LO. 2006b. Chemical Constituents of Galium tortumense. Turk J Chem. 30: 515-523.
Hanna REB, Foster FI, Brennan GP. 2013. Fasciola hepatica: Histological demonstration of apoptosis in the reproductive organs of flukes of triclabendazole-sensitive and triclabendazole-resistant isolates, and in field-derived flukes from triclabendazole-treated hosts, using in situ hybridisation to visualise endonuclease- generated DNA stand breaks. Vete Paracytol. 191: 240-251.
Harborne JB. 1973. Phytochemicals methods. Chapman and Hill, London.
Hopkins WG. 1999. Introduction to plant physiology. John Wiley, New York, USA pp 298-292.
Hosseini R, Mulligan BJ. 2002. Application of rice (Oryza sativa L.) suspension culture in studying senescence in vitro (I). Single strand preferring nuclease activity. Electro J Biotech. 5: 42-54.
Inone I, Suzuki R, Koide T, Sakaguchi N, Ogihara Y,Yabu Y. 1994. Antioxidant, gallic acid, induces apoptosis in HL-60RG cells. Biochem Biophys Res Commun. 204: 898–904.
Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N. 2002. The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci. 115: 973–982.
Jones AM. 2001. Programmed cell death in development and defense. Plant Physiol. 125:94-97.
Kara?sma?lo?lu, M.C. (2017) Investigation of the antimitotic and antimutagenic effects of methanolic extracts of Pyracantha coccinea. Turk J Life Sci. 2(1):110-116.
Karmous I, Chaoui A, Jaouani Kh Sheehan D, Ferjani E, Scoccianti V, Crinelli R. 2014. Role of the ubiquitin proteasome pathway and some peptidases during seed germination and copper stress in bean cotyledons. Plant Physiol Biochem. 76: 77-85.
Kaufman PB, Leland J, Warber CS, James A, Harry D, Brielmann L. 1999. Natural products from plants. CRC Press, London pp.1581-1589.
Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nat. 227:680-685.
Langston JB, Bai S, Jones LM. 2005. Increases in DNA fragmentation and induction of a senescence-specific nuclease are delayed during corolla senescence in ethylene insensitive (etr1-1) transgenic petunias. J Exper Bot. 56: 15–23.
Liu Y, Zhou C, Qiu C, LU X, Wang Y. 2013. Chlorogenic acid induced apoptosis and inhibition of proliferation in human acute promyelocytic leukemia HL 60 cells. Mol Med Rep. 8: 1106-1110.
Lombardi L, Ceccarelli N, Picciarelli P, Lorenzi R. 2007. DNA degradation during programmed cell death in Phaseolus coccineus suspor. Plant Physiol Biochem. 45(3-4):221-227.
Lowe S.W. Lin AW. 2000. Apoptosis in cancer. Carcinogen. 21:485–495.
Madeo F, Fröhlich E, Fröhlich KU. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol. 139: 729–734.
Mahavorasirikul W, Viyanant V, Chaijaroenkul W, Itharat, A, Bangchang K. 2010. Cytotoxic activity of Thai medicinal plants against human cholangiocarcinoma, laryngeal and hepatocarcinoma cells in vitro. BMC Complement Altern Med. 10:55.
McCollum G, Keng PC, States JC, McCabe MJ. 2005. Arsenite delays progression through each cell cycle phase and induces apoptosis following G2/M arrest in U937 myeloid leukemia cells. J Pharmacol Exp Ther. 313:877–887.
Murata T, Sano T, Sasabe M, Nonaka Sh, Higashiyama T, Hasezawa S, Machida Y, Hasebe M. 2013. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat Comm. 4:1967 doi: 10.1038/ncomms2967.
Newman DJ, Cragg GM, Snader KM. 2002. Natural products as a source of new drugs over the period. J Nat Prod 66:1022-1037.
Ning SB, Wang L, Song YC. 2002. Identification of programmed cell death in situ in individual plant cells in vivo using a chromosome preparation technique. J Exp Bot. 53: 651-658.
Pal SK, Shukla Y. 2003. Herbal medicine: current status and the future. Asian Pac J Cancer Prev. 4(4):281-288.
Park HJ, Kim MJ, Ha E, Chung JH. 2008. Apoptotic effect of hesperidin through caspase3 activation in human colon cancer cells, SNU-C4. Phytomed. 15:147–151.
Pelayo RH, Pincheira J, Gimenez-Abian JF. Clarke DJ, Connsuelo T. 2003. P53-Independent checkpoint controls in a plant cell model. Biol Res. 36: 381-388.
Reddy BS, Wang CX, Samaha H, Lubet, R, Steele, VE, Kelloff GJ, Rao CV. 1997. Chemoprevention of colon carcinogenesis by dietary perillyl alcohol. Cancer Res. 57: 420–425.
Reed JC, Pellecchia M. 2005. Apoptosis-based therapies for hematologic malignancies. Blood 106: 408–418.
Renxian W, Liu Sh, Wang J, Dong Q, Xu L, Rui Q. 2013. Purification, characterization, and identification of a senescence related serine protease in dark-induced senescent wheat leaves. Phytochem. 95: 118-126.
Reynolds E. 1963. The use of lead citrate at a high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 17: 208-212.
Safarzadeh E, Shotorbani S, Baradaran B. 2014. Herbal medicine as inducers of apoptosis in Cancer Treatment. Adv Pharm Bull. 4(Suppl 1): 421–427.
Sakamoto W, Takami T. 2014. Nucleases in higher plants and their possible involvement in DNA degradation during leaf senescence. J Exper Bot. 65(14): 3835–3843.
Schmidt M, Scholz CJ, Gavril GL, Otto C, Polednik C, Roller J, Hagen R. 2014a. Effect of Galium verum aqueous extract on growth, motility and gene expression in drug-sensitive and-resistant laryngeal carcinoma cell lines. Int J Oncol. 44:745–760.
Schmidt M, Polednik C, Roller J, Hagen R. 2014b. Galium verum aqueous extract strongly inhibits the motility of head and neck cancer cell lines and protects mucosal keratinocytes against toxic DNA damage. Oncol Rep. 32:1296–1302.
Schwartz BW. 1992. Insect muscle as a model for programmed cell death. J Neurobiol. 23:1312-1326.
Shah JV, Cleveland DW. 2000. Waiting for anaphase. Mad2 and the spindle assembly checkpoint. Cell. 103:997-1000.
Shahid M, Wang J, Gu X, Chen W, Ali T, Gao J, Han D, Yang R, Fanning S, Han B. 2017. Prototheca zopfii induced ultrastructural features associated with apoptosis in bovine mammary epithelial cells. Front Cell Infect Microbiol. 7:299, doi.org/10.3389/fcimb.2017.00299
Shalini R, Velavan S. 2017. Evaluation of antimitotic activity of Aplotaxis auriculata rhizomes using Allium cepa root meristamatic cells. Ind J Appl Res. 7(12): 315-317.
Smith-Hall C, Larsen HO, Pouliot M. 2012. People, plants, and health: a conceptual framework for assessing changes in medicinal plant consumption. J Ethnobiol Ethnomed. 8:43, doi: 10.1186/1746-4269-8-43.
Sodmergen KS, Tano S, Kuroiwa T. 1991. Degradation of chloroplast DNA in second leaves of rice (Oryza sativa) before leaf yellowing. Protopl. 160:89-98.
Stevenson DE, Hurst RD. 2007. Polyphenolic phytochemicals - just antioxidants or much more? Cell Mol Life Sci. 64:2900-2916.
Tada Y, Hata S, Takata Y, Nakayashiki, H, Tosa Y, Mayama S. 2001. Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant-Microbe Interact. 14: 477–486.
Taraphdar AK, Roy M, Bhattacharya RK. 2001. Natural products as inducers of apoptosis: Implication for cancer therapy and prevention. Cur Sci. 80 (11): 1387-1396.
Tariq A, Sadia S, Pan K, Ullah I, Mussarat S, Sun F, Abiodun OO, Batbaatar A, Li Z, Song D et al. 2017. A systematic review on ethnomedicines of anticancer plants. Phytother Res. 31: 202–264.
Tawab SAF, Adam ZM, Sobieh Sh. 2014. Assessment of Punica granatum L. extract on the mitotic arrest of plant bioassay system. Life Sci J. 11(8):757-770.
Tawab SAF, Adam ZM, Sobieh Sh. 2004. Suppression of mitotic process associated with metaphase arrest of Allium cepa L. roots using. I. Rosmarinus officinalis L. Water extract. Int J Agri Biol. 6: 690-698.
Vaux DL, Korsmeyer SJ. 1999. Cell death in development. Cell. 96: 245–254.
Vichai V, Kirtikara K. 2006. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 1:1112-1116.
Wang IK, Lin-Shiau SY, Lin JK. 1999. Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells. Eur J Cancer. 35: 1517–1525.
Yan?k F, Aytürk V, Vardar F. 2017. Programmed cell death evidence in wheat (Triticum aestivum L.) roots induced by aluminum oxide (Al2O3) nanoparticles. Caryol. 70(2):112-119.
You BR, Park WH. 2010. Gallic acid-induced lung cancer cell death is related to glutathione depletion as well as reactive oxygen species increase. Toxicol in Vitro. 24:1356-1362.
Yupsanis T, Symeonidis L, Kalemi T, Moustaka H, Yupsani A. 2004. Purification, properties and specificity of an endonuclease from Agropyron elongatum seedlings. Plant Physiol Biochem. 42: 795–802.
Zhang H, Zhong X, Zhang X, Shang D, Zhou Y, Zhang C. 2016. Enhanced anticancer effect of abt-737 in combination with naringenin on gastric cancer cells. Exp Ther Med. 11: 669–673.
Zhou BB, Elledge SJ. 2000. The DNA damage response. Putting checkpoints in perspective. Nat. 408:433-439.
Amirghofran Z, Bahmani M, Azadmehr A, Javidnia K. 2006a. Induction of apoptosis in leukemia cell lines by Linum persicum and Euphorbia cheiradenia. J Cancer Res Clin Oncol. 132:427-432.
Amirghofran Z, Bahmani M, Azadmehr A, Javidnia K. 2006b. Anticancer effects of various Iranian native medicinal plants on human tumor cell lines. Neoplasma. 53: 428–433.
Aslantürk ÖS, Çelik TA, Karabey B, Karabey F. 2017. Active phytochemical detecting, antioxidant, cytotoxic, apoptotic activities of ethyl acetate and methanol extracts of Galium aparine L. British J Pharmaceutal Res. 15(6): 1-16.
Avila J, Devarenne TP. 2013. Ubiquitination of the tomato cell suppressor Adi3 by the Ring E3 ubiquitin ligase AdBil. Biochem Bioph Reas Comm. 430: 119-124.
Bao L, Liu F, Guo HB, Li Y, Tan BB, Zhang WX, Peng YH. 2016. Naringenin inhibits proliferation, migration, and invasion as well as induces apoptosis of gastric cancer sgc7901 cell line by downregulation of akt pathway. Tumor Biol. 37: 11365–11374.
Blank A, Mckeon TA. 1989. Single-strand preferring nuclease activity in wheat leaves is increased in senescence and is negatively photoregulated. Proc Nat Aca Sci USA. 86: 3169-3173.
Chen H, Miao Q, Geng M, Liu J, Hu Y, Tian L, Pan J, Yang Y. 2013. Anti-Tumor effect of rutin on human neuroblastoma cell lines through inducing G2/ M cell cycle arrest and promoting apoptosis. The Sci World J. 2013, Article ID 269165, 8 pages.
Cragg GM, Kingston DG, Newman DJ. 2005. Anticancer agents from natural products. Taylor and Francis Group; Brunner Routledge Psychology Press, London.
Domínguez F, Moreno J, Cejudo F. 2004. A Gibberellin-induced nuclease is localized in the nucleus of wheat aleurone cells undergoing programmed cell death. The J Biol Chem. 279 (12): 11530–11536.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation method for small quantities of fresh tissues. Phytoch Bull Bota Society Amm. 19:11–15.
El-Gamal AA, Halim AF, Amer MM, Saad HA, Takeya K, Itokawa H. 1999. Flavonol glycosides from Galium sinaicum. Alex J Pharm Sci. 13 (1): 41-47.
Farr KA, Cohen-Fix O. 1999. The metaphase to anaphase transition. Euro J Biochem. 263:1-14.
Fiskesj? G. 1997. Allium test for screening chemicals; evaluation of cytologic parameters. In: Wang W, Gorsuch JW, Hughes JS. editors. Plants for environmental studies. CRC Lewis Publishers, Boca Raton, New York, pp 308–333.
Fuzinatto VA, Pagliarini MS, Valle CB. 2007. Evidence of programmed cell death during microsporogenesis in an interspecific Brachiaria (Poaceae: Panicoideae: Paniceae) hybrid. Gent Mol Res. 6: 308- 315.
Gao Y, Ma Q, Ma YB, Ding L, Xu XL, Wei DF, Wei L, Zhang JW. 2018. Betulinic acid induces apoptosis and ultrastructural changes in MDA-MB-231 breast cancer cells. Ultrastruct Pathol. 42(1):49-54.
Gîrd C, Costea T, Nencu I, Popescu ML, Du?u LE. 2015. Phytochemical and phytobiological research upon aerial parts and seeds from Peucedanum officinale. Farmacia. 63(2): 247-253.
Gli?ska S, Gabara B. 2000. Localization of selenium deposits in meristematic cells of Allium sativum L. roots treated with selenium salts. Folia Histochem Cytobiol 38:143–147.
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE. 2001. Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta. 212: 205–214.
Güvenalp Z, Kazaz C, Kaya Y, Demirezer LO. 2006a. Phytochemical investigation on Galium humifusum growing in Turkey. Biochem Syst Ecol. 34:894-89.
Güvenalp Z, Kilic N, Kazaz C, Kaya Y, Demirezer LO. 2006b. Chemical Constituents of Galium tortumense. Turk J Chem. 30: 515-523.
Hanna REB, Foster FI, Brennan GP. 2013. Fasciola hepatica: Histological demonstration of apoptosis in the reproductive organs of flukes of triclabendazole-sensitive and triclabendazole-resistant isolates, and in field-derived flukes from triclabendazole-treated hosts, using in situ hybridisation to visualise endonuclease- generated DNA stand breaks. Vete Paracytol. 191: 240-251.
Harborne JB. 1973. Phytochemicals methods. Chapman and Hill, London.
Hopkins WG. 1999. Introduction to plant physiology. John Wiley, New York, USA pp 298-292.
Hosseini R, Mulligan BJ. 2002. Application of rice (Oryza sativa L.) suspension culture in studying senescence in vitro (I). Single strand preferring nuclease activity. Electro J Biotech. 5: 42-54.
Inone I, Suzuki R, Koide T, Sakaguchi N, Ogihara Y,Yabu Y. 1994. Antioxidant, gallic acid, induces apoptosis in HL-60RG cells. Biochem Biophys Res Commun. 204: 898–904.
Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N. 2002. The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci. 115: 973–982.
Jones AM. 2001. Programmed cell death in development and defense. Plant Physiol. 125:94-97.
Kara?sma?lo?lu, M.C. (2017) Investigation of the antimitotic and antimutagenic effects of methanolic extracts of Pyracantha coccinea. Turk J Life Sci. 2(1):110-116.
Karmous I, Chaoui A, Jaouani Kh Sheehan D, Ferjani E, Scoccianti V, Crinelli R. 2014. Role of the ubiquitin proteasome pathway and some peptidases during seed germination and copper stress in bean cotyledons. Plant Physiol Biochem. 76: 77-85.
Kaufman PB, Leland J, Warber CS, James A, Harry D, Brielmann L. 1999. Natural products from plants. CRC Press, London pp.1581-1589.
Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nat. 227:680-685.
Langston JB, Bai S, Jones LM. 2005. Increases in DNA fragmentation and induction of a senescence-specific nuclease are delayed during corolla senescence in ethylene insensitive (etr1-1) transgenic petunias. J Exper Bot. 56: 15–23.
Liu Y, Zhou C, Qiu C, LU X, Wang Y. 2013. Chlorogenic acid induced apoptosis and inhibition of proliferation in human acute promyelocytic leukemia HL 60 cells. Mol Med Rep. 8: 1106-1110.
Lombardi L, Ceccarelli N, Picciarelli P, Lorenzi R. 2007. DNA degradation during programmed cell death in Phaseolus coccineus suspor. Plant Physiol Biochem. 45(3-4):221-227.
Lowe S.W. Lin AW. 2000. Apoptosis in cancer. Carcinogen. 21:485–495.
Madeo F, Fröhlich E, Fröhlich KU. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol. 139: 729–734.
Mahavorasirikul W, Viyanant V, Chaijaroenkul W, Itharat, A, Bangchang K. 2010. Cytotoxic activity of Thai medicinal plants against human cholangiocarcinoma, laryngeal and hepatocarcinoma cells in vitro. BMC Complement Altern Med. 10:55.
McCollum G, Keng PC, States JC, McCabe MJ. 2005. Arsenite delays progression through each cell cycle phase and induces apoptosis following G2/M arrest in U937 myeloid leukemia cells. J Pharmacol Exp Ther. 313:877–887.
Murata T, Sano T, Sasabe M, Nonaka Sh, Higashiyama T, Hasezawa S, Machida Y, Hasebe M. 2013. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat Comm. 4:1967 doi: 10.1038/ncomms2967.
Newman DJ, Cragg GM, Snader KM. 2002. Natural products as a source of new drugs over the period. J Nat Prod 66:1022-1037.
Ning SB, Wang L, Song YC. 2002. Identification of programmed cell death in situ in individual plant cells in vivo using a chromosome preparation technique. J Exp Bot. 53: 651-658.
Pal SK, Shukla Y. 2003. Herbal medicine: current status and the future. Asian Pac J Cancer Prev. 4(4):281-288.
Park HJ, Kim MJ, Ha E, Chung JH. 2008. Apoptotic effect of hesperidin through caspase3 activation in human colon cancer cells, SNU-C4. Phytomed. 15:147–151.
Pelayo RH, Pincheira J, Gimenez-Abian JF. Clarke DJ, Connsuelo T. 2003. P53-Independent checkpoint controls in a plant cell model. Biol Res. 36: 381-388.
Reddy BS, Wang CX, Samaha H, Lubet, R, Steele, VE, Kelloff GJ, Rao CV. 1997. Chemoprevention of colon carcinogenesis by dietary perillyl alcohol. Cancer Res. 57: 420–425.
Reed JC, Pellecchia M. 2005. Apoptosis-based therapies for hematologic malignancies. Blood 106: 408–418.
Renxian W, Liu Sh, Wang J, Dong Q, Xu L, Rui Q. 2013. Purification, characterization, and identification of a senescence related serine protease in dark-induced senescent wheat leaves. Phytochem. 95: 118-126.
Reynolds E. 1963. The use of lead citrate at a high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 17: 208-212.
Safarzadeh E, Shotorbani S, Baradaran B. 2014. Herbal medicine as inducers of apoptosis in Cancer Treatment. Adv Pharm Bull. 4(Suppl 1): 421–427.
Sakamoto W, Takami T. 2014. Nucleases in higher plants and their possible involvement in DNA degradation during leaf senescence. J Exper Bot. 65(14): 3835–3843.
Schmidt M, Scholz CJ, Gavril GL, Otto C, Polednik C, Roller J, Hagen R. 2014a. Effect of Galium verum aqueous extract on growth, motility and gene expression in drug-sensitive and-resistant laryngeal carcinoma cell lines. Int J Oncol. 44:745–760.
Schmidt M, Polednik C, Roller J, Hagen R. 2014b. Galium verum aqueous extract strongly inhibits the motility of head and neck cancer cell lines and protects mucosal keratinocytes against toxic DNA damage. Oncol Rep. 32:1296–1302.
Schwartz BW. 1992. Insect muscle as a model for programmed cell death. J Neurobiol. 23:1312-1326.
Shah JV, Cleveland DW. 2000. Waiting for anaphase. Mad2 and the spindle assembly checkpoint. Cell. 103:997-1000.
Shahid M, Wang J, Gu X, Chen W, Ali T, Gao J, Han D, Yang R, Fanning S, Han B. 2017. Prototheca zopfii induced ultrastructural features associated with apoptosis in bovine mammary epithelial cells. Front Cell Infect Microbiol. 7:299, doi.org/10.3389/fcimb.2017.00299
Shalini R, Velavan S. 2017. Evaluation of antimitotic activity of Aplotaxis auriculata rhizomes using Allium cepa root meristamatic cells. Ind J Appl Res. 7(12): 315-317.
Smith-Hall C, Larsen HO, Pouliot M. 2012. People, plants, and health: a conceptual framework for assessing changes in medicinal plant consumption. J Ethnobiol Ethnomed. 8:43, doi: 10.1186/1746-4269-8-43.
Sodmergen KS, Tano S, Kuroiwa T. 1991. Degradation of chloroplast DNA in second leaves of rice (Oryza sativa) before leaf yellowing. Protopl. 160:89-98.
Stevenson DE, Hurst RD. 2007. Polyphenolic phytochemicals - just antioxidants or much more? Cell Mol Life Sci. 64:2900-2916.
Tada Y, Hata S, Takata Y, Nakayashiki, H, Tosa Y, Mayama S. 2001. Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant-Microbe Interact. 14: 477–486.
Taraphdar AK, Roy M, Bhattacharya RK. 2001. Natural products as inducers of apoptosis: Implication for cancer therapy and prevention. Cur Sci. 80 (11): 1387-1396.
Tariq A, Sadia S, Pan K, Ullah I, Mussarat S, Sun F, Abiodun OO, Batbaatar A, Li Z, Song D et al. 2017. A systematic review on ethnomedicines of anticancer plants. Phytother Res. 31: 202–264.
Tawab SAF, Adam ZM, Sobieh Sh. 2014. Assessment of Punica granatum L. extract on the mitotic arrest of plant bioassay system. Life Sci J. 11(8):757-770.
Tawab SAF, Adam ZM, Sobieh Sh. 2004. Suppression of mitotic process associated with metaphase arrest of Allium cepa L. roots using. I. Rosmarinus officinalis L. Water extract. Int J Agri Biol. 6: 690-698.
Vaux DL, Korsmeyer SJ. 1999. Cell death in development. Cell. 96: 245–254.
Vichai V, Kirtikara K. 2006. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 1:1112-1116.
Wang IK, Lin-Shiau SY, Lin JK. 1999. Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells. Eur J Cancer. 35: 1517–1525.
Yan?k F, Aytürk V, Vardar F. 2017. Programmed cell death evidence in wheat (Triticum aestivum L.) roots induced by aluminum oxide (Al2O3) nanoparticles. Caryol. 70(2):112-119.
You BR, Park WH. 2010. Gallic acid-induced lung cancer cell death is related to glutathione depletion as well as reactive oxygen species increase. Toxicol in Vitro. 24:1356-1362.
Yupsanis T, Symeonidis L, Kalemi T, Moustaka H, Yupsani A. 2004. Purification, properties and specificity of an endonuclease from Agropyron elongatum seedlings. Plant Physiol Biochem. 42: 795–802.
Zhang H, Zhong X, Zhang X, Shang D, Zhou Y, Zhang C. 2016. Enhanced anticancer effect of abt-737 in combination with naringenin on gastric cancer cells. Exp Ther Med. 11: 669–673.
Zhou BB, Elledge SJ. 2000. The DNA damage response. Putting checkpoints in perspective. Nat. 408:433-439.
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2021-10-08
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Sobieh, S. S., & Fahmy, D. M. (2021). Assessment of antimitotic and programmed cell death stimulation potentials of Galium sinaicum (Delile ex Decne) Boiss. at the cellular level. Caryologia, 74(2), 21–35. https://doi.org/10.36253/caryologia-1057
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Copyright (c) 2021 Dr/ Shaimaa Selmi Sobieh
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