Hemangiosarcoma in rodents: Mode-of-action evaluation and human relevance

Toxicological Sciences

Volumn 111, Issue 1, 2009, Pages 4-18

  Cohen, Samuel M ^a   Storer, Richard D ^b   Criswell, Kay A ^c   Doerrer, Nancy G ^d   Dellarco, Vicki L ^e   Pegg, David G ^f   Wojcinski, Zbigniew W ^g   Malarkey, David E ^h   Jacobs, Abigail C ⁱ   Klaunig, James E ^j   Swenberg, James A ^k   Cook, Jon C ^c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c PFIZER INC   (United States)

^d ILSI HEALTH AND ENVIRONMENTAL SCIENCES INSTITUTE   (United States)

^e U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^f Michigan Technology and Research Institute   (United States)

^g Fulcrum Pharma Developments Inc   (United States)

^h NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

ⁱ CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^j INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k UNIVERSITY OF NORTH CAROLINA   (United States)

more..

Author keywords

Angiogenesis; Endothelial cells; Endothelial precursor cells; Hemangiosarcoma; Human relevance; Mode of action; PPAR agonists

Indexed keywords

2 BUTOXYETHANOL; 4 CHLOROANILINE; 4 NITROANILINE; CARBARIL; CD34 ANTIGEN; CONNECTIVE TISSUE GROWTH FACTOR; DRONEDARONE; ENTECAVIR; FENRETINIDE; FIBROBLAST GROWTH FACTOR; OLANZAPINE; PENTOSAN POLYSULFATE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PREGABALIN; RETINOIC ACID RECEPTOR; SCATTER FACTOR; TADALAFIL; THORIUM DIOXIDE; TRANSFORMING GROWTH FACTOR BETA; TROGLITAZONE; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VILDAGLIPTIN; VINYL CHLORIDE;

ADIPOCYTE; ANGIOGENESIS; ANGIOSARCOMA; CARCINOGENESIS; CARCINOGENICITY; CELL ACTIVATION; CELL GROWTH; CYTOKINE RELEASE; DNA DAMAGE; DOG; DOWN REGULATION; DRUG PROTEIN BINDING; ENDOTHELIUM CELL; ERYTHROPOIESIS; EXPERIMENTAL RAT; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTOXICITY; HEMATOPOIETIC STEM CELL; HEMOLYSIS; HUMAN; HYPOXEMIA; MACROPHAGE ACTIVATION; MISSENSE MUTATION; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; RESPIRATION DEPRESSION; REVIEW; SIGNAL TRANSDUCTION; SPECIES COMPARISON; SPECIES DIFFERENCE;

ANIMALS; CARCINOGENS; DNA; DOGS; HEMANGIOSARCOMA; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; RATS; RISK ASSESSMENT; SPECIES SPECIFICITY; VINYL CHLORIDE;

CANIS FAMILIARIS; MUS; RATTUS; RODENTIA;

EID: 69049088861     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp131     Document Type: Review

References (100)

1. Abbot, R., and Palmieri, C. (2008). Angiosarcoma of the breast following surgery and radiotherapy for breast cancer. Nat. Clin. Pract. Oncol. 5, 727-736.
2. Abdo, K. M., Johnson, J. D., and Nyska, A. (2003). Toxicity and carcinogenicity of Elmiron in F344/N rats and B6C3F1 mice following 2 years of gavage administration. Arch. Toxicol. 77, 702-711.
3. Amaral, M. C., Miles, S., Kumar, G., and Nel, A. E. (1993). Oncostatin-M stimulates tyrosine protein phosphorylation in parallel with the activation of p42MAPK/ERK-2 in Kaposi's cells. Evidence that this pathway is important in Kaposi cell growth. J. Clin. Invest. 92 848-857.
4. Barillari, G., and Ensoli, B. (2002). Angiogenic effects of extracellular human immunodeficiency virus type 1 Tat protein and its role in the pathogenesis of AIDS-associated Kaposi's sarcoma. Clin. Microbiol. Rev. 15, 310-326.
5. Berger, J., Bailey, P., Biswas, C., Cullinan, C. A., Doebber, T. W., Hayes, N. S., Saperstein, R., Smith, R. G., and Leibowitz, M. D. (1996). Thiazolidinediones produce a conformational change in peroxisomal proliferator-activated receptor-gamma: Binding and activation correlate with antidiabetic actions in db/db mice. Endocrinology 137, 4189-4195.
6. Bigot-Lasserre, D., Chuzel, F., Debruyne, E., Urtizberea, M., and Carmichael, N. (2000). Tumorigenic potential of carbaryl in the P53 knockout mouse model. The Toxicologist 54, 1038.
7. Bishop-Bailey, D., and Hla, T. (1999). Endothelial cell apoptosis induced by the peroxisome proliferator-activated receptor (PPAR) ligand 15-dioxy-Δ12, 14-prostaglandin J2. J. Biol. Chem. 274, 17042-17048.
8. Boobis, A. R., Cohen, S. M., Dellarco, V., McGregor, D., Meek, M. E., Vickers, C., Willcocks, D., and Farland, W. (2006). IPCS framework for analyzing the relevance of a cancer mode of action for humans. Crit. Rev. Toxicol. 36, 781-792.
9. Boobis, A. R., Doe, J. E., Heinrich-Hirsch, B., Meek, M. E., Munn, S., Ruchirawat, M., Schlatter, J., Seed, J., and Vickers, C. (2008). IPCS framework for analyzing the relevance of a noncancer mode of action for humans. Crit. Rev. Toxicol. 38, 87-96.
10. Breider, M. A., Gough, A. W., Haskins, J. R., Sobocinski, G., and de la Iglesia, F. A. (1999). Troglitazone-induced heart and adipose tissue cell proliferation in mice. Toxicol. Pathol. 27, 545-552.
11. Bristow, R. G., and Hill, R. P. (2008). Hypoxia, DNA repair, and genetic instability. Nat. Rev. 8, 180-192.
12. Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936.
13. Cave, M., Falkner, K., Patel, M., Reynolds, L., Barve, S., and McClain, C. (2008a). Biomarkers for vinyl chloride-induced hepatic hemangiosarcoma. Hemangiosarcoma in Rodents: Mode-of-Action Evaluation and Human Relevance, Society of Toxicology Contemporary Concepts in Toxicology Workshop, December 4-5, 2008 (Abstract). Available at: http://www.toxicology.org/ai/meet/SOT-CCT08_WkshpMaterials.pdf
14. Cave, M., Falkner, K., Patel, M., Reynolds, L., Barve, S., and McClain, C. (2008b). Vinyl chloride-induced hepatic hemangiosarcoma: The Louisville experience. Hemangiosarcoma in Rodents: Mode-of-Action Evaluation and Human Relevance, Society of Toxicology Contemporary Concepts in Toxicology Workshop, December 4-5, 2008 (Abstract). Available at: http://www.toxicology.org/ai/meet/ SOT-CCT08_WkshpMaterials.pdf
15. Cohen, A. D., Cagnano, E., and Vardy, D. A. (2001). Cherry angiomas associated with exposure to bromides. Dermatology 202, 52-53.
16. Cohen, S. M., and Ellwein, L. B. (1991). Genetic errors, cell proliferation, and carcinogenesis. Cancer Res. 51, 6493-6505.
17. Corthals, S. M., Kamendulis, L. M., and Klaunig, J. E. (2006). Mechanisms of 2-butoxyethanol-induced HS. Toxicol. Sci. 92, 378-386.
18. Criswell, K. A. (2008). Epigenetic mode of action associated with induction of hemangiosarcoma in mice treated with pregabalin. Hemangiosarcoma in Rodents: Mode-of-Action Evaluation and Human Relevance, Society of Toxicology Contemporary Concepts in Toxicology Workshop. December 4-5, 2008 (Abstract). Available at: http://www.toxicology.org/ai/meet/SOT-CCT08_WkshpMaterials.pdf
19. Cromwell, J. A., and Goldenthal, E. I. (2006). Hemangiosarcomas induced in mice by N-(4-hydrophenyl)retinamide. The Toxicologist 90, 428 (Abstract #2088).
20. Crossno, J. T., Jr., Majka, S. M., Grazia, T., Gill, R. G., and Klemm, D. J. (2006). Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J. Clin. Invest. 116, 3220-3228.
21. DeFelipe, I., and Redondo, P. (1998). Eruptive angiomas after treatment with cyclosporine in a patient with psoriasis. Arch. Dermatol. 134, 1487-1488.
22. Dickerson, E. B., Thomas, R., Fosmire, S. P., Lamerato-Kozicki, A. R., Bianco, S. R., Wojcieszyn, J. W., Breen, M., Helfand, S. C., and Modiano, J. F. (2005). Mutations of phosphatase and tensin homolog deleted from chromosome 10 in canine HS. Vet. Pathol. 42, 618-632.
23. Ding, T. T., Kumar, S., and Yu, D. C. (2008). The role of endothelial progenitor cells in tumour vasculogenesis. Pathology 75, 265-273.
24. Duddy, S. K., Gorospe, S. M., Bleavins, M. R., and de la Iglesia, F. A. (1999b). Spontaneous and thiazolidinedione-induced B6C3F1 mouse hemangiosarcomas exhibit low ras oncogene mutation frequencies. Toxicol. Appl. Pharmacol. 160, 133-140.
25. Duddy, S. K., Parker, R. F., Bleavins, M. R., Gough, A. W., Rowse, P. E., Gorospe, S., Dethloff, L. A., and de la Iglesia, F. A. (1999a). P53 is not inactivated in B6C3F1 mouse vascular tumors arising spontaneously or associated with long-term administration of the thiazolidinedione troglitazone. Toxicol. Appl. Pharmacol. 156, 106-122.
26. Elwell, M. R., Mahler, J. F., and Ruecker, F. A. (2004). Proliferative and non-proliferative lesions in the heart and vasculature in mice, MCV-1. In Guides for Toxicologic Pathology. STP/ARP/AFIP, Washington, DC.
27. Emadi, S. N., Hosseini-Khalili, A., Soroush, M. R., Davoodi, S. M., and Aghamiri, S. S. (2008). Mustard gas scarring with specific pigmentary, trophic and vascular characteristics (case report, 16-year post-exposure). Ecotoxicol. Environ. Saf. 69, 574-576.
28. European Medicines Agency (EMEA). (2006a). CHMP SWP Reflection Paper on PPARs (Peroxisome Proliferator Activated Receptors). EMEA/341972/ 2006, September 2006, London.
29. European Medicines Agency (EMEA). (2006b). Withdrawal Public Assessment Report of the Marketing Authorisation Application for Multaq (Dronedarone). EMEA/CHMP/370798, 18 October 2006, London.
30. European Medicines Agency (EMEA). (2007). European Public Assessment Report (EPAR) Galvus. EMEA/H/C/771, London.
31. Ferrara, N. (2002). VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer 2, 795-803.
32. Ferrara, N., and Kerbel, R. S. (2005). Angiogenesis as a therapeutic target. Nature 15, 967-974.
33. Firooz, A., Komeili, A., and Dowlati, Y. (1999). Eruptive melanocytic nevi and cherry angiomas secondary to exposure to sulfur mustard gas. J. Am. Acad. Dermatol. 40, 646-647.
34. Foellmi-Adams, L. A., Wyse, B. M., Herron, D., Nedergaard, J., and Kletzien, R. F. (1996). Induction of uncoupling protein in brown adipose tissue. Synergy between norepinephrine and pioglitazone, an insulin-sensitizing agent. Biochem. Pharmacol. 52, 693-701.
35. Foellmi-Adams, L. A., Wyse, B. M., Herron, D., Nedergaard, J., and Kletzien, R. F. (2004). Congenital disorder of oxygen sensing: Association of the homozygous Chuvash polycythemia VHL mutation with thrombosis and vascular abnormalities but not tumors. Blood 103 3924-3932.
36. Fukumura, D., Ushiyama, A., Duda, D. G., Xu, L., Tam, J., Krishna, V., Chatterjee, K., Garkavtsev, I., and Jain, R. K. (2003). Paracrine regulation of angiogenesis and adipocyte differentiation during in vivo adipogenesis. Circ. Res. 93, 88-97.
37. Goodman, D. (1991). Expert Panel to Review the Safety and Toxicity of 4-Hydroxyphenyl Retinamide. D. Goodman, Chairperson. Summary Conclusions. National Institutes of Health, Bethesda, MD. September 5, 1991.
38. Gordeuk, V. R., Sergueeva, A. I., Miasnikova, G. Y., Okhotin, D., Voloshin, Y., Choyke, P. L., Butman, J. A., Jedlickova, K., Prchal, J. T., and Polyakova, L. A. (2004). Congenital disorder of oxygen sensing: Association of the homozygous Chuvash polycythemia VHL mutation with thrombosis and vascular abnormalities but not tumors. Blood 103 3924-3932.
39. Grommes, C., Landreth, G. E., and Heneka, M. T. (2004). Antineoplastic effects of peroxisome proliferator-activated receptor γ agonists. Lancet Oncol. 5, 419-429.
40. Hardisty, J. F., Elwell, M. R., Ernst, H., Greaves, P., Kolenda-Roberts, H., Malarkey, D. E., Mann, P. C., and Tellier, P. A. (2007). Histopathology of hemangiosarcomas in mice and hamsters and liposarcomas/ fibrosarcomas in rats associated with PPAR agonists. Toxicol. Pathol. 35, 928-941.
41. Harris, A. L. (2002). Hypoxia - A key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47.
42. Haseman, J. K., Hailey, J. R., and Morris, R. W. (1998). Spontaneous neoplasm incidences in Fischer 344 rats and B6C3F1 mice in two-year carcinogenicity studies: A National Toxicology Program update. Toxicol. Pathol. 26, 428-441.
43. Hefazi, M., Maleki, M., Mahmoudi, M., Tabatabaee, A., and Balali-Mood, M. (2006). Delayed complications of sulfur mustard poisoning in the skin and the immune system of Iranian veterans 16-20 years after exposure. Int. J. Dermatol. 45, 1025-1031.
44. Herman, J. R., Dethloff, L. A., McGuire, E. J., Parker, R. F., Walsh, K. M., Gough, A. W., Masuda, H., and de la Iglesia, F. A. (2002). Rodent carcinogenicity with the thiazolidinedione antidiabetic agent troglitazone. Toxicol. Sci. 68, 226-236.
45. Hickey, M. M., Lam, J. C., Bezman, N. A., Rathmell, W. K., and Simon, M. C. (2007). Von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2α signaling erythropoiesis. J. Clin. Invest. 117, 3879-3889.
46. Hutley, L. J., Herington, A. C., Shurety, W., Cheung, C., Vesey, D. A., Cameron, D. P., and Prins, J. B. (2001). Human adipose tissue endothelial cells promote preadipocyte proliferation. Am. J. Endocrinol. Metab. 281, E1037-E1044.
47. Igarashi, A., Hayashi, N., Nashiro, K., and Takehara, K. (1998). Differential expression of connective tissue growth factor gene in cutaneous fibrohistiocytic and vascular tumors. J. Cutaneous Pathol. 25, 143-148.
48. Jacobs, A. C. (2008). Hemangiosarcoma and pharmaceuticals: An FDA perspective. Hemangiosarcoma in Rodents: Mode-of-Action Evaluation and Human Relevance, Society of Toxicology Contemporary Concepts in Toxicology Workshop. December 4-5, 2008 (Abstract). Available at: http://www.toxicology.org/ai/meet/SOT-CCT08_WkshpMaterials.pdf
49. Jinnin, M., Medici, D., Park, L., Limaye, N., Liu, Y., Boscolo, E., Bischoff, J., Vikkula, M., Boye, E., and Olsen, B. R. (2008). Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat. Med. 14, 1236-1246.
50. Johnson, T. E. (2008). Retinoid-induced hemangiosarcoma in mice: potential insight from in vivo and in vitro studies. Hemangiosarcoma in rodents: Mode-of-Action Evaluation and Human Relevance, Society of Toxicology Contemporary Concepts in Toxicology Workshop, December 4-5, 2008 (Abstract). Available at: http://www.toxicology.org/ai/meet/SOT-CCT08_WkshpMaterials.pdf
51. Kakiuchi-Kiyota, S., Vetro, J. A., Suzuki, S., Varney, M. L., Han, H., Nascimento, M., Pennington, K. L., Arnold, L. L., Singh, R. K., and Cohen, S. M. (2009). Effect of the PPARγ agonist troglitazone on endothelial cells in vivo and in vitro: Differences between human and mouse. Toxicol. Appl. Pharmacol. 237, 83-90.
52. Kerbel, R., and Folkman, J. (2002). Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer 2, 727-739.
53. Kershaw, E. E., and Flier, J. S. (2004). Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 89, 2548-2556.
54. Kielhorn, J., Melber, C., Wahnschaffe, U., Aitio, A., and Mangelsdorf, I. (2000). Vinyl chloride: Still a cause for concern. Environ. Health Perspect. 108, 579-588.
55. Klaunig, J. E., and Kamendulis, L. M. (2005). Mode of action of butoxyethanol-induced mouse liver HS and hepatocellular carcinomas. Toxicol. Lett. 156, 107-115.
56. Kojiro, M., Nakashima, T., Ito, Y., Ikezaki, H., Mori, T., and Kido, C. (1985). Thorium dioxide-related angiosarcoma of the liver. Pathomorphologic study of 29 autopsy cases. Arch. Pathol. Lab. Med. 109, 853-857.
57. Laifenfeld, D., Gilchrist, A., Drubin, D., Jorge, M., Eddy, S. F., Elliston, K. O., Obert, L. A., Sokowloski, S. A.,Gosink, M.M.,Cook, J. C., et al. (2009). The role of hypoxia in 2-butoxyethanol-induced hemangiosarcoma. Toxicol. Sci. (in press).
58. Lamerato-Kozicki, A. R., Helm, K. M., Jubala, C. M., Cutter, G. C., and Modiano, J. F. (2006). Canine hemangiosarcoma originates from hematopoietic precursors with potential for endothelial differentiation. Exp. Hematol. 34, 870-878.
59. Lanza, F.,Healy, L., and Sutherland, D.R. (2001). Structural and functional features of the CD34 antigen: An update. J. Biol. Regul. Homeost. Agents 15, 1-13.
60. Lazennec, G., and Jorgensen, C. (2008). Concise review: Adult multipotent stromal cells and cancer: Risk or benefit? Stem Cells 26, 1387-1394.
61. Ma, H. J., Zhao, G., Shi, F., and Wang, Y. X. (2006). Eruptive cherry angiomas associated with vitiligo: Provoked by topical nitrogen mustard? J. Dermatol. 33, 877-879.
62. Maehama, T., Taylor, G., and Dixon, J. (2001). PTEN and myotubularin: Novel phosphoinositide phosphatases. Annu. Rev. Biochem. 70, 247-259.
63. Meek, M. E., Bucher, J. R., Cohen, S. M., Dellarco, V., Hill, R. N., Lehman-McKeeman, L. D., Longfellow, D. G., Pastoor, T., Seed, J., and Patton, D. E. 2003). A framework for human relevance analysis of information on carcinogenic modes of action. Crit. Rev. Toxicol. 33, 591-653.
64. 2,3-ethenoguanine in rat brain and liver after exposure to vinyl chloride. Cancer Res. 62, 5183-5188.
65. Moyer, C., Allen, D., Basabe, A., Maronpot, R. R., and Nyska, A. (2004). Analysis of vascular endothelial growth factor (VEGF) and a receptor subtype (KDR/flk-1) in the liver of rats exposed to riddelliine: A potential role in the development of hemangiosarcomas. Exp. Toxicol. Pathol. 55, 455-465.
66. Murata, T., Hata, Y., Ishibashi, T., Kim, S., Hsueh, W. A., Law, R. E., and Hinton, D. R. (2001). Response of experimental retinal neovascularization to thiazolidinediones. Arch. Ophthalmol. 119 709-717.
67. Nyberg, P., Xie, L., and Kalluri, R. (2005). Endogenous inhibitors of angiogenesis. Cancer Res. 65, 3967-3979.
68. Nyska,A., Haseman, J. K., Kohen, R., and Maronpto, R. R. (2004).Association of liver hemangiosarcoma and secondary iron overload in B6C3F1 mice. The National Toxicology Program experience. Toxicol. Pathol 32, 222-228.
69. Nyska, A., Moomaw, C. R., Foley, J. F., Maronpot, R. R., Malarkey, D. E., Cummings, C. A., Peddada, S., Moyer, C. F., Allen, D. G., Travlos, G., and Chan, P. C. (2002). The hepatic endothelial carcinogen riddelliine induces endothelial apoptosis, mitosis, S phase, and p53 and hepatocytic vascular endothelial growth factor expression after short-term exposure. Toxicol. Appl. Pharmacol. 184, 153-164.
70. Ohnishi, T., Arnold, L. L., Clark, N. M., Wisecarver, J. L., and Cohen, S. M. (2007). Comparison of endothelial cell proliferation in normal liver and adipose tissue in B6C3F1 mice, F344 rats, and humans. Toxicol. Pathol. 35, 904-909.
71. Okuno, A., Tamemoto, H., Tobe, K., Ueki, K., Mori, Y., Iwamoto, K., Umesono, K., Akanuma, Y., Fujiwara, T., Horikoshi, H., et al. (1998). Troglitazone increases the number of small adipocytes without the change of white adipose tissue mass in obese Zucker rats. J. Clin. Invest. 101, 1354-1361.
72. Park, J., Kamendulis, L. M., and Klaunig, J. E. (2002). Effects of 2-butoxyethanol on hepatic oxidative damage. Toxicol. Lett. 126 19-29.
73. Pegg, D. G., Wojcinski, Z., Criswell, K., Herman, J., and Anderson, T. (2006). Epigenetic mode of action associated with induction of hemangiosarcoma in mice. The Toxicologist 90, 334.
74. Pezzolesi, M. G., Platzer, P., Waite, K. A., and Eng, C. (2008). Differential expression of PTEN-targeting microRNAs miR-19a and miR-21 in Cowden syndrome. Am. J. Hum. Genet. 82, 1141-1149.
75. Physician's Desk Reference Electronic Library. (2009). Thomson Micromedex. Available at: www.thomsonhc.com. Accessed February 2, 2009.
76. Priester, W. A., and McKay, F. W. (1980). The occurrence of tumors in domestic animals. Natl. Cancer Inst. Monogr. 54, 1-210.
77. Raymond, L. W., Williford, L. S., and Burke, W. A. (1998). Eruptive cherry angiomas and irritant symptoms after one acute exposure to the glycol ether solvent 2-butoxyethanol. J. Occup. Environ. Med. 40, 1059-1064.
78. Requena, L., and Sangueza, O. P. (1997). Cutaneous vascular proliferations. Part II. Hyperplasias and benign neoplasms. J. Am. Acad. Dermatol. 37, 887-922.
79. Rogers, M. S., and D'Amato, R. J. (2006). The effect of genetic diversity on angiogenesis. Exp. Cell Res. 312, 561-574.
80. Rogers, M. S., Rohan, R. M., Birsner, A. E., and D'Amato, R. J. (2003). Genetic loci that control vascular endothelial growth factor-induced angiogenesis. FASEB J. 17, 2112-2114.
81. Rogers, M. S., Rohan, R. M., Birsner, A. E., and D'Amato, R. J. (2004). Genetic loci that control the angiogenic response to basic fibroblast growth factor. FASEB J. 18, 1050-1059.
82. Rosner, M., Hanneder, M., Siegel, N., Valli, A., Fuchs, C., and Hengstschlager, M. (2008). The mTOR pathway and its role in human genetic diseases. Mutat. Res. 659, 284-292.
83. Ruben, Z., Arceo, R. J., Bishop, S. P., Elwell, M. R., Kerns, W. D., Mesfin, G. M., Sandusky, G. E., and Van Vleet, J. F. (1997). Proliferative lesions of the heart and vasculature in rats, CD-1. In Guides for Toxicologic Pathology. STP/ARP/AFIP, Washington, DC.
84. Rupnick, M. A., Panigrahy, D., Zhang, C. Y., Dallabrida, S. M., Lowell, B. B., Langer, R., and Folkman, M. J. (2002). Adipose tissue mass can be regulated through the vasculature. Proc. Natl. Acad. Sci. U. S. A. 99, 10730-10735.
85. Sears, I. B., MacGinnitie, M. A., Kovacs, L. G., and Graves, R. A. (1996). Differentiation-dependent expression of the brown adipocyte uncoupling protein gene: Regulation by peroxisome proliferator-activated receptor gamma. Mol. Cell. Biol. 16, 3410-3419.
86. Seed, J., Carney, E. W., Corley, R. A., Crofton, K. M., DeSesso, J. M., Foster, P. M., Kavlock, R., Kimmel, G., Klaunig, J., Meek, M. E., et al. (2005). Using mode of action and life stage information to evaluate the human relevance of animal toxicity data. Crit. Rev. Toxicol. 35, 663-672.
87. Shaked, Y., Bertolini, F., Man, S., Rogers, M. S., Cervi, D., Foutz, T., Rawn, K., Voskas, D., Dumont, D. J., Ben-David, Y., et al. (2005). Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis: Implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 7, 101-111.
88. Sierra-Honigmann, M. R., Nath, A. K., Murakami, C., García-Cardeña, G., Papapetropoulos, A., Sessa, W. C., Madge, L. A., Schechner, J. S., Schwabb, M. B., Polverini, P. J., and Flores-Riveros, J. R. (1998). Biological action of leptin as an angiogenic factor. Science 281, 1683-1686.
89. Sonich-Mullin, C., Fielder, R., Wiltse, J., Baetcke, K., Dempsey, J., Fenner-Crisp, P.,Grant,D.,Hartley,M.,Knaap,A.,Kroese,D., et al. (2001). IPCS-Mode of action of chemical carcinogenesis. Regul. Toxicol. Pharmacol. 34, 146-152.
90. Stienstra, R., Duval, C., Keshtkar, S., van der Laak, J., Kersten, S., and Müller, M. (2008). Peroxisome proliferator-activated receptor γ activation promotes infiltration of alternatively activated macrophages into adipose tissue. J. Biol. Chem. 283, 22620-22627.
91. Tafuri, S. R. (1996). Troglitazone enhances differentiation, basal glucose uptake, and Glu1 protein levels in 3T3-L1 adipocytes. Endocrinology 137, 4706-4712.
92. Tai, T. A., Jennermann, C., Brown, K. K., Oliver, B. B., MacGinnitie, M. A., Wilkison, W. O., Brown, H. R., Lehmann, J. M., Kliewer, S. A., Morris, D. C., and Graves, R. A. (1996). Activation of the nuclear receptor peroxisome proliferator-activated receptor gamma promotes brown adipocyte differentiation. J. Biol. Chem. 271, 29909-29914.
93. Tannehill-Gregg, S. H., Sanderson, T. P., Minnema, D., Voelker, R., Ulland, B., Cohen, S. M., Arnold, L. L., Schilling, B. E., Waites, C. R., and Dominick, M. A. (2007). Rodent carcinogenicity profile of the antidiabetic dual PPAR γ and α agonist muraglitazar. Toxicol. Sci. 98, 258-270.
94. U.S. Environmental Protection Agency (US EPA). (2004). EPA Interim Registration Eligibility Decision (IRED), Carbaryl. Washington, DC: US Environmental Protection Agency, Office of Prevention, Pesticide, and Toxic Substances, Case 0080.
95. Van Oosterhout, J. P., Van der Laan, J. W., De Waal, E. J., Olejniczak, K., Hilgenfeld, M., Schmidt, V., and Bass, R. (1997). The utility of two rodent species in carcinogenic risk assessment of pharmaceuticals in Europe. Regul. Toxicol. Pharmacol. 25, 6-17.
96. Virtanen, A., Pukkala, E., and Auvinen, A. (2007). Angiosarcoma after radiotherapy: A cohort study of 332,163 Finnish cancer patients. Br. J. Cancer 97, 115-117.
97. Waites, C. R., Dominick, M. A., Sanderson, T. P., and Schilling, B. E. (2007). Nonclinical safety evaluation of muraglitazar, a novel PPAR α/γ agonist. Toxicol. Sci. 100, 248-258.
98. Weiss, S. W., and Goldblum, J. R. (2008a). Benign tumors and tumor-like lesions of blood vessels. In Enzinger and Weiss's Soft Tissue Tumors 5th ed. (S. W. Weis and J. R. Goldblum, Eds.), pp. 633-679. Mosley Elsevier, China.
99. Weiss, S. W., and Goldblum, J. R. (2008b). Malignant vascular tumors. In Enzinger and Weiss's Soft Tissue Tumors, 5th ed. (S. W. Weis and J. R. Goldblum, Eds.), pp. 703-732. Mosley Elsevier, China.
100. Werner, C., Kamani, C. H., Gensch, C., Böhm, M., and Laufs, U. (2007). The peroxisome proliferator-activated receptor-γ agonist pioglitazone increases number and function of endothelial progenitor cells in patients with coronary artery disease and normal glucose tolerance. Diabetes 56, 2609-2615.