Microgravity alters cancer growth and progression

Current Cancer Drug Targets

Volumn 14, Issue 4, 2014, Pages 394-406

  Jhala, Dhwani V ^a   Kale, Raosaheb K ^a,b   Singh, Rana P ^a,b  

^a CENTRAL UNIVERSITY OF GUJARAT   (India)

^b JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Apoptosis; Cancer growth; Cell proliferation; Cell signalling; Microgravity

Indexed keywords

OSTEOPONTIN; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN;

APOPTOSIS; BIOCHEMISTRY; CANCER GROWTH; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SIGNALING ASSAY; HUMAN; MICROGRAVITY; NONHUMAN; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CARCINOGENESIS; CELLULAR IMMUNITY; CYTOSKELETON; DISEASE COURSE; EXTRACELLULAR MATRIX; GENETIC EPIGENESIS; IMMUNOLOGY; METABOLISM; MICROSATELLITE INSTABILITY; NEOPLASMS; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME; WEIGHTLESSNESS;

ANIMALS; APOPTOSIS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOSKELETON; DISEASE PROGRESSION; EPIGENESIS, GENETIC; EXTRACELLULAR MATRIX; HUMANS; IMMUNITY, CELLULAR; MICROSATELLITE INSTABILITY; MODELS, BIOLOGICAL; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR BURDEN; WEIGHTLESSNESS;

EID: 84903694283     PISSN: 15680096     EISSN: 18735576     Source Type: Journal    
DOI: 10.2174/1568009614666140407113633     Document Type: Review

References (88)

1. Strollo, F. Hormonal changes in humans during spaceflight. Adv. Space Biol. Med. 1999, 7, 99-129.
2. Cogoli, A. Hematological and immunological changes during space flight. Acta Astronaut. 1981, 8 (9-10), 995-1002.
3. De Santo, N. G.; Cirillo, M.; Kirsch, K. A.; Correale, G.; Drummer, C.; Frassl, W.; Perna, A. F.; Di Stazio, E.; Bellini, L.; Gunga, H. C. Anemia and erythropoietin in space flights. Semin. Nephrol. 2005, 25 (6), 379-387.
4. Kim, M. H. Y.; George, K. A.; Cucinotta, F. A. Evaluation of skin cancer risk for lunar and Mars missions. Adv. Space Res. 2006, 37 (9), 1798-1803.
5. Barr, Y. R.; Bacal, K.; Jones, J. A.; Hamilton, D. R. Breast cancer and spaceflight: Risk and management. Aviat. Space Environ. Med. 2007, 78 (4 II), A26-A37.
6. Ingram, M.; Techy, G. B.; Saroufeem, R.; Yazan, O.; Narayan, K. S.; Goodwin, T. J.; Spaulding, G. F. Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In Vitro Cell. Dev. Biol.-Animal 1997, 33 (6), 459-466.
7. Becker, J. L.; Souza, G. R. Using space-based investigations to inform cancer research on Earth. Nat. Rev. Cancer 2013, 13 (5), 315-327.
8. Lelièvre, S. A.; Weaver, V. M.; Nickerson, J. A.; Larabell, C. A.; Bhaumik, A.; Petersen, O. W.; Bissell, M. J. Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proc. Natl. Acad. Sci. U. S. A. 1998, 95 (25), 14711-14716.
9. Roskelley, C. D.; Desprez, P. Y.; Bissell, M. J. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. U. S. A. 1994, 91 (26), 12378-12382.
10. Chiquet, M.; Renedo, A. S.; Huber, F.; Flück, M. How do fibroblasts translate mechanical signals into changes in extracellular matrix production? Matrix Biol. 2003, 22 (1), 73-80.
11. Adams, J. C.; Watt, F. M. Regulation of development and differentiation by the extracellular matrix. Development 1993, 117 (4), 1183-1198.
12. Hagios, C.; Lochter, A.; Bissell, M. J. Tissue architecture: The ultimate regulator of epithelial function? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1998, 353 (1370), 857-870.
13. Merker, H. J. Morphology of the basement membrane. Microsc. Res. Tech. 1994, 28 (2), 95-124.
14. Carson, D. D. Extracellular matrix: forum introduction. Reprod. Biol. Endocrinol. 2004, 2, 1.
15. Lindberg, U.; Karlsson, R.; Lassing, I.; Schutt, C. E.; Höglund, A. S. The microfilament system and malignancy. Semin. Cancer Biol. 2008, 18 (1), 2-11.
16. Friedman, E.; Verderame, M.; Winawer, S.; Pollack, R. Actin cytoskeletal organization loss in the benign-to-malignant tumor transition in cultured human colonic epithelial cells. Cancer Res. 1984, 44 (7), 3040-3050.
17. Ulbrich, C.; Pietsch, J.; Grosse, J.; Wehland, M.; Schulz, H.; Saar, K.; Hubner, N.; Hauslage, J.; Hemmersbach, R.; Braun, M.; van Loon, J.; Vagt, N.; Egli, M.; Richter, P.; Einspanier, R.; Sharbati, S.; Baltz, T.; Infanger, M.; Ma, X.; Grimm, D. Differential gene regulation under altered gravity conditions in follicular thyroid cancer cells: relationship between the extracellular matrix and the cytoskeleton. Cell Physiol. Biochem. 2011, 28 (2), 185-198.
18. Sanders, A. J.; Ye, L.; Mason, M. D.; Jiang, W. G. The impact of EPLIN (epithelial protein lost in neoplasm) on endothelial cells, angiogenesis and tumorigenesis. Angiogenesis 2010, 13 (4), 317-326.
19. Ferrari, S.; Battini, R.; Kaczmarek, L.; Rittling, S.; Calabretta, B.; de Riel, J. K.; Philiponis, V.; Wei, J. F.; Baserga, R. Coding sequence and growth regulation of the human vimentin gene. Mol. Cell. Biol. 1986, 6 (11), 3614-3620.
20. Infanger, M.; Kossmehl, P.; Shakibaei, M.; Bauer, J.; Kossmehl-Zorn, S.; Cogoli, A.; Curcio, F.; Oksche, A.; Wehland, M.; Kreutz, R.; Paul, M.; Grimm, D. Simulated weightlessness changes the cytoskeleton and extracellular matrix proteins in papillary thyroid carcinoma cells. Cell Tissue Res. 2006, 324 (2), 267-277.
21. Grimm, D.; Bauer, J.; Kossmehl, P.; Shakibaei, M.; Schonberger, J.; Pickenhahn, H.; Schulze-Tanzil, G.; Vetter, R.; Eilles, C.; Paul, M.; Cogoli, A. Simulated microgravity alters differentiation and increases apoptosis in human follicular thyroid carcinoma cells. FASEB J. 2002, 16 (6), 604-606.
22. Schnee, J. M.; Hsueh, W. A. Angiotensin II, adhesion, and cardiac fibrosis. Cardiovasc. Res. 2000, 46 (2), 264-268.
23. Mukherjee, B. B.; Nemir, M.; Beninati, S.; Cordella-Miele, E.; Singh, K.; Chackalaparampil, I.; Shanmugam, V.; DeVouge, M. W.; Mukherjee, A. B. Interaction of osteopontin with fibronectin and other extracellular matrix molecules. Ann. N. Y. Acad. Sci. 1995, 760, 201-212.
24. Khan, S. A.; Lopez-Chua, C. A.; Zhang, J.; Fisher, L. W.; Sorensen, E. S.; Denhardt, D. T. Soluble osteopontin inhibits apoptosis of adherent endothelial cells deprived of growth factors. J. Cell. Biochem. 2002, 85 (4), 728-736.
25. Kossmehl, P.; Schonberger, J.; Shakibaei, M.; Faramarzi, S.; Kurth, E.; Habighorst, B.; Von Bauer, R.; Wehland, M.; Kreutz, R.; Infanger, M.; Schulze-Tanzil, G.; Paul, M.; Grimm, D. Increase of fibronectin and osteopontin in porcine hearts following ischemia and reperfusion. J. Mol. Med. 2005, 83 (8), 626-637.
26. Kawata, M.; Sekiya, S.; Kera, K.; Kimura, H.; Takamizawa, H. Neural rosette formation within in vitro spheroids of a clonal human teratocarcinoma cell line, PA-1/NR: Role of extracellular matrix components in the morphogenesis. Cancer Res. 1991, 51 (10), 2655-2669.
27. Grimm, D.; Bauer, J.; Hofstadter, F.; Riegger, G. A. J.; Kromer, E. P. Characteristics of multicellular spheroids formed by primary cultures of human thyroid tumor cells. Thyroid 1997, 7 (6), 859-865.
28. Nederman, T.; Norling, B.; Glimelius, B.; Carlsson, J.; Brunk, U. Demonstration of an extracellular matrix in multicellular tumor spheroids. Cancer Res. 1984, 44 (7), 3090-3097.
29. Vassy, J.; Portet, S.; Beil, M.; Millot, G.; Fauvel-Lafeve, F.; Gasset, G.; Schoevaert, D. Weightlessness acts on human breast cancer cell line MCF-7. Adv. Space Res. 2003, 32 (8), 1595-1603.
30. Qian, A. R.; Zhang, W.; Xie, L.; Weng, Y.; Yang, P.; Wang, Z.; Hu, L.; Xu, H.; Tian, Z.; Shang, P. Simulated weightlessness alters biological characteristics of human breast cancer cell line MCF-7. Acta Astronaut. 2008, 63 (7-10), 947-958.
31. Clejan, S.; O'Connor, K. C.; Cowger, N. L.; Cheles, M. K.; Haque, S.; Primavera, A. C. Effects of simulated microgravity on DU145 human prostate carcinoma cells. Biotechnol. Bioeng. 1996, 50 (5), 587-597.
32. Yi, Z. C.; Xia, B.; Xue, M.; Zhang, G. Y.; Wang, H.; Zhou, H. M.; Sun, Y.; Zhuang, F. Y. Simulated microgravity inhibits the proliferation of K562 erythroleukemia cells but does not result in apoptosis. Adv. Space Res. 2009, 44 (2), 233-244.
33. Rijken, P. J.; de Groot, R. P.; Kruijer, W.; de Laat, S. W.; Verkleij, A. J.; Boonstra, J. Identification of specific gravity sensitive signal transduction pathways in human A431 carcinoma cells. Adv. Space Res. 1992, 12 (1), 145-152.
34. Moes, M. J. A.; Gielen, J. C.; Bleichrodt, R. J.; Van Loon, J. J. W. A.; Christianen, P. C. M.; Boonstra, J. Simulation of microgravity by magnetic levitation and random positioning: Effect on human A431 cell morphology. MiST. 2011, 23 (2), 249-261.
35. Stark, H. J.; Baur, M.; Breitkreutz, D.; Mirancea, N.; Fusenig, N. E. Organotypic keratinocyte cocultures in defined medium with regular epidermal morphogenesis and differentiation. J. Invest. Dermatol. 1999, 112 (5), 681-691.
36. Griffith, L. G.; Swartz, M. A. Capturing complex 3D tissue physiology in vitro. Nat. Rev. Mol. Cell Biol. 2006, 7 (3), 211-224.
37. Marrero, B.; Messina, J. L.; Heller, R. Generation of a tumor spheroid in a microgravity environment as a 3D model of melanoma. In Vitro Cell. Dev. Biol.-Animal 2009, 45 (9), 523-534.
38. Vassy, J.; Portet, S.; Beil, M.; Millot, G.; Fauvel-Lafeve, F.; Karniguian, A.; Gasset, G.; Irinopoulou, T.; Calvo, F.; Rigaut, J. P.; Schoevaert, D. The effect of weightlessness on cytoskeleton architecture and proliferation of human breast cancer cell line MCF-7. FASEB J. 2001, 15 (6), 1104-1106.
39. Coinu, R.; Chiaviello, A.; Galleri, G.; Franconi, F.; Crescenzi, E.; Palumbo, G. Exposure to modeled microgravity induces metabolic idleness in malignant human MCF-7 and normal murine VSMC cells. FEBS Lett. 2006, 580 (10), 2465-2470.
40. Fu, H.; Subramanian, R. R.; Masters, S. C. 14-3-3 Proteins: Structure, function, and regulation. In Annu. Rev. Pharmacol. Toxicol. 2000, 40, 617-647.
41. Vincent, L.; Avancena, P.; Cheng, J.; Rafii, S.; Rabbany, S. Y. Simulated microgravity impairs leukemic cell survival through altering VEGFR-2/VEGF-A signaling pathway. Ann. Biomed. Eng. 2005, 33 (10), 1405-1410.
42. Zou, L. X.; Cui, S. Y.; Zhong, J.; Yi, Z. C.; Sun, Y.; Fan, Y. B.; Zhuang, F. Y. Simulated microgravity induce apoptosis and downregulation of erythropoietin receptor of UT-7/EPO cells. Adv. Space Res. 2010, 46 (10), 1237-1244.
43. Takeda, M.; Magaki, T.; Okazaki, T.; Kawahara, Y.; Manabe, T.; Yuge, L.; Kurisu, K. Effects of simulated microgravity on proliferation and chemosensitivity in malignant glioma cells. Neurosci. Lett. 2009, 463 (1), 54-59.
44. Dorward, A.; Sweet, S.; Moorehead, R.; Singh, G. Mitochondrial contributions to cancer cell physiology: Redox balance, cell cycle, and drug resistance. J. Bioenerg. Biomembr. 1997, 29 (4), 385-392.
45. Yang, C.; Li, Y.; Zhang, Z.; Luo, C.; Tong, Y.; Zhou, G.; Xie, P.; Hu, J.; Li, G. Effects of space flight exposure on cell growth, tumorigenicity and gene expression in cancer cells. Adv. Space Res. 2008, 42 (12), 1898-1905.
46. Kumei, Y.; Nakajima, T.; Sato, A.; Kamata, N.; Enomoto, S. Reduction of G1 phase duration and enhancement of c-myc gene expression in HeLa cells at hypergravity. J. Cell Sci. 1989, 93 (2), 221-226.
47. Jessup, J. M.; Frantz, M.; Sonmez-Alpan, E.; Locker, J.; Skena, K.; Waller, H.; Battle, P.; Nachman, A.; Weber, M. E.; Thomas, D. A.; Curbeam R.L, Jr.; Baker, T. L.; Goodwin, T. J. Microgravity culture reduces apoptosis and increases the differentiation of a human colorectal carcinoma cell line. In Vitro Cell. Dev. Biol.-Animal 2000, 36 (6), 367-373.
48. Taga, M.; Yamauchi, K.; Odle, J.; Furian, L.; Sundaresan, A.; Ramesh, G. T.; Pellis, N. R.; Andrassy, R. J.; Kulkarni, A. D. Melanoma growth and tumorigenicity in models of microgravity. Aviat. Space Environ. Med. 2006, 77 (11), 1113-1116.
49. Nakamura, K.; Kuga, H.; Morisaki, T.; Baba, E.; Sato, N.; Mizumoto, K.; Sueishi, K.; Tanaka, M.; Katano, M. Simulated microgravity culture system for a 3-D carcinoma tissue model. Biotechniques 2002, 33 (5), 1068-1076.
50. Becker, J. L.; Prewett, T. L.; Spaulding, G. F.; Goodwin, T. J. Three-dimensional growth and differentiation of ovarian tumor cell line in high aspect rotating-wall vessel: Morphologic and embryologic considerations. J. Cell. Biochem. 1993, 51 (3), 283-289.
51. Reya, T.; Morrison, S. J.; Clarke, M. F.; Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414 (6859), 105-111.
52. Leszczyniecka, M.; Roberts, T.; Dent, P.; Grant, S.; Fisher, P. B. Differentiation therapy of human cancer: basic science and clinical applications. Pharmacol. Ther. 2001, 90 (2-3), 105-156.
53. Jessup, J. M.; Brown, D.; Fitzgerald, W.; Ford, R. D.; Nachman, A.; Goodwin, T. J.; Spaulding, G. Induction of carcinoembryonic antigen expression in a three-dimensional culture system. In Vitro Cell. Dev. Biol.-Animal 1997, 33 (5), 352-357.
54. De Groot, R. P.; Rijken, P. J.; Den Hertog, J.; Boonstra, J.; Verkleij, A. J.; De Laat, S. W.; Kruijer, W. Microgravity decreases c-fos induction and serum response element activity. J. Cell Sci. 1990, 97 (1), 33-38.
55. Kossmehl, P.; Shakibaei, M.; Cogoli, A.; Infanger, M.; Curcio, F.; Schonberger, J.; Eilles, C.; Bauer, J.; Pickenhahn, H.; Schulze-Tanzil, G.; Paul, M.; Grimm, D. Weightlessness induced apoptosis in normal thyroid cells and papillary thyroid carcinoma cells via extrinsic and intrinsic pathways. Endocrinology 2003, 144 (9), 4172-4179.
56. Kossmehl, P.; Shakibaei, M.; Cogoli, A.; Pickenhahn, H.; Paul, M.; Grimm, D. Simulated microgravity induces programmed cell death in human thyroid carcinoma cells. J. Gravit. Physiol. 2002, 9 (1), 295-296.
57. Minowada, G.; Welch, W. J. Clinical implications of the stress response. J. Clin. Invest. 1995, 95 (1), 3-12.
58. St. Croix, B. Florenes, V. A. Rak, J. W. Flanagan, M. Bhattacharya, N. Slingerland, J. M. Kerbel, R. S. Impact of the cyclin-dependent kinase inhibitor p27(Kip1) on resistance of tumor cells to anticancer agents. Nat. Med. 1996, 2 (11), 1204-1210.
59. Sasaki, N.; Morisaki, T.; Hashizume, K.; Yao, T.; Tsuneyoshi, M.; Noshiro, H.; Nakamura, K.; Yamanaka, T.; Uchiyama, A.; Tanaka, M.; Katano, M. Nuclear factor-kappaB p65 (RelA) transcription factor is constitutively activated in human gastric carcinoma tissue. Clin. Cancer Res. 2001, 7 (12), 4136-4142.
60. Grosse, J.; Wehland, M.; Pietsch, J.; Schulz, H.; Saar, K.; Hubner, N.; Eilles, C.; Bauer, J.; Abou-El-Ardat, K.; Baatout, S.; Ma, X.; Infanger, M.; Hemmersbach, R.; Grimm, D. Gravity-sensitive signaling drives 3-dimensional formation of multicellular thyroid cancer spheroids. FASEB J. 2012, 26 (12), 5124-5140.
61. Pietsch, J.; Riwaldt, S.; Bauer, J.; Sickmann, A.; Weber, G.; Grosse, J.; Infanger, M.; Eilles, C.; Grimm, D. Interaction of proteins identified in human thyroid cells. Int. J. Mol. Sci. 2013, 14 (1), 1164-1178.
62. Liu, Y.; Wang, E. Transcriptional analysis of normal human fibroblast responses to microgravity stress. Genomics Proteomics Bioinformatics 2008, 6 (1), 29-41.
63. Hollander, J.; Gore, M.; Fiebig, R.; Mazzeo, R.; Ohishi, S.; Ohno, H.; Ji, L. L. Spaceflight downregulates antioxidant defense systems in rat liver. Free Radic. Biol. Med. 1998, 24 (2), 385-390.
64. Kalmar, B.; Greensmith, L. Induction of heat shock proteins for protection against oxidative stress. Adv. Drug Del. Rev. 2009, 61 (4), 310-318.
65. Razmara, A.; Sunday, L.; Stirone, C.; Xiao, B. W.; Krause, D. N.; Duckles, S. P.; Procaccio, V. Mitochondrial effects of estrogen are mediated by ERα in brain endothelial cells. J. Pharmacol. Exp. Ther. 2008, 325 (3), 782-790.
66. Lu, N.; Wang, W.; Liu, J.; Wong, C. W. Protein kinase C epsilon affects mitochondrial function through estrogen-related receptor alpha. Cell. Signal. 2011, 23 (9), 1473-1478.
67. Zheng, H.; Tian W.; Yan H.; Jiang H.; Liu S.; Yue L.; Han F.; Wei L.; Chen X.; Li, Y. Expression of estrogen receptor α in human breast cancer cells regulates mitochondrial oxidative stress under simulated microgravity. Adv. Space Res. 2012, 49, 1432-1440.
68. Testard, I.; Ricoul, M.; Hoffschir, F.; Flury-Herard, A.; Dutrillaux, B.; Fedorenko, B.; Gerasimenko, V.; Sabatier, L. Radiationinduced chromosome damage in astronauts' lymphocytes. Int. J. Radiat. Biol. 1996, 70, 403-411.
69. Yang, T. C.; George, K.; Johnson, A. S.; Durante, M.; Fedorenko, B. S. Biodosimetry results from space flight Mir-18. Radiat. Res. 1997, 148, S17-S23.
70. Ikenaga, M.; Hirayama, J.; Kato, T.; Kitao, H.; Han, Z. B.; Ishizaki, K.; Nishizawa, K.; Suzuki, F.; Cannon, T. F.; Fukui, K.; Shimazu, T.; Kamigaichi, S.; Ishioka, N.; Matsumiya, H. Effect of space flight on the frequency of micronuclei and expression of stressresponsive proteins in cultured mammalian cells. J. Radiat. Res. (Tokyo) 2002, 43, S141-S147.
71. Okaichi, K.; Ide, M.; Usui, A.; Okumura, Y. Hypergravity induces phosphorylation of p53 at serine 15, but not an expression of p53-downstream genes. J. Radiat. Res. (Tokyo) 2004, 45 (3), 399-403.
72. Chakrabarty, S.; Jan, Y.; Brattain, M. G.; Tobon, A.; Varani, J. Diverse cellular responses elicited from human colon carcinoma cells by transforming growth factor-beta. Cancer Res. 1989, 49 (8), 2112-2117.
73. Howell, G. M.; Humphrey, L. E.; Awwad, R. A.; Wang, D.; Koterba, A.; Periyasamy, B.; Yang, J.; Li, W.; Willson, J. K. V.; Ziober, B. L.; Coleman, K.; Carboni, J.; Lynch, M.; Brattain, M. G. Aberrant regulation of transforming growth factor-alpha during the establishment of growth arrest and quiescence of growth factor independent cells. J. Biol. Chem. 1998, 273 (15), 9214-9223.
74. Wang, D.; Li, W.; Jiang, W.; Humphrey, L. E.; Howell, G. M.; Brattain, M. G. Autocrine TGF-a expression in the regulation of initiation of human colon carcinoma growth. J. Cell. Physiol. 1998, 177 (3), 387-395.
75. Dias, S.; Hattori, K.; Heissig, B.; Zhu, Z.; Wu, Y.; Witte, L.; Hicklin, D. J.; Tateno, M.; Bohlen, P.; Moore, M. A. S.; Rafii, S. Inhibition of both paracrine and autocrine VEGF/VEGFR-2 signaling pathways is essential to induce long-term remission of xenotransplanted human leukemias. Proc. Natl. Acad. Sci. U. S. A. 2001, 98 (19), 10857-10862.
76. Dias, S.; Choy, M.; Alitalo, K.; Rafii, S. Vascular endothelial growth factor (VEGF)-C signaling through FLT-4 (VEGFR-3) mediates leukemic cell proliferation, survival, and resistance to chemotherapy. Blood 2002, 99 (6), 2179-2184.
77. Zou, L. X.; Cui, S. Y.; Zhong, J.; Yi, Z. C.; Sun, Y.; Fan, Y. B.; Zhuang, F. Y. Upregulation of erythropoietin receptor in UT-7/EPO cells inhibits simulated microgravity-induced cell apoptosis. Adv. Space Res. 2011, 48 (2), 390-394.
78. Sytkowski, A. J.; Davis, K. L. Erythroid cell growth and differentiation in vitro in the simulated microgravity environment of the nasa rotating wall vessel bioreactor. In Vitro Cell. Dev. Biol.-Animal 2001, 37 (2), 79-83.
79. Schlessinger, J.; Schreiber, A. B.; Levi, A.; Lax, I.; Libermann, T.; Yarden, Y. Regulation of cell proliferation by epidermal growth factor. CRC Crit. Rev. Biochem. 1983, 14 (2), 93-111.
80. Carpenter, G.; Cohen, S. Epidermal growth factor. Annu. Rev. Biochem. 1979, 48, 193-216.
81. Imler, J. L.; Wasylyk, B. AP1, a composite transcription factor implictted in abnormal growth control. Prog. Growth Factor Res. 1989, 1 (2), 69-77.
82. Muller, R.; Wagner, E. F. Differentiation of F9 teratocarcinoma stem cells after transfer of c-fos proto-oncogenes. Nature 1984, 311 (5985), 438-442.
83. De Groot, R. P.; Kruyt, F. A. E.; Van Der Saag, P. T.; Kruijer, W. Ectopic expression of c-jun leads to differentiation of P19 embryonal carcinoma cells. EMBO J. 1990, 9 (6), 1831-1837.
84. Verma, I. M.; Sassone-Corsi, P. Proto-oncogenes fos: Complex but versatile regulation. Cell 1987, 51 (4), 513-514.
85. De Groot, R. P.; Rijken, P. J.; Boonstra, J.; Verkleij, A. J.; De Laat, S. W.; Kruijer, W. Epidermal growth factor-induced expression of c-fos is influenced by altered gravity conditions. Aviat. Space Environ. Med. 1991, 62 (1), 37-40.
86. Gilman, M. Z.; Wilson, R. N.; Weinberg, R. A. Multiple proteinbinding sites in the 5'-flanking region regulate c-fos expression. Mol. Cell. Biol. 1986, 6 (12), 4305-4316.
87. Treisman, R. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors. Cell 1986, 46 (4), 567-574.
88. Han, Z. B.; Ishizaki, K.; Nishizawa, K.; Kato, T.; Todo, T.; Ikenaga, M. A Genetic effect of altered gravity: Mutations induced by simulated hypogravity and hypergravity in microsatellite sequences of human tumor cells. Mutat. Res. 1999, 426 (1), 1-10.