Chronic Delivery of a Thrombospondin-1 Mimetic Decreases Skeletal Muscle Capillarity in Mice

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Audet, Gerald N ^a   Fulks, Daniel ^a   Stricker, Janelle C ^a   Olfert, I Mark ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; N ACETYLSARCOSYLGLYCYLVALYL DEXTRO ALLOISOLEUCYLTHREONYLNORVALYLISOLEUCYLARGINYLPROLINE ETHYLAMIDE; THROMBOSPONDIN 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG MECHANISM; GASTROCNEMIUS MUSCLE; IN VIVO STUDY; MALE; MORPHOMETRICS; MOUSE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; OSMOTIC PUMP; PLANTARIS MUSCLE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE CAPILLARITY; SOLEUS MUSCLE;

ANIMALS; ANTIGENS, CD36; APOPTOSIS; BIOMIMETIC MATERIALS; CAPILLARY ACTION; DRUG DELIVERY SYSTEMS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; PHYSICAL CONDITIONING, ANIMAL; RUNNING; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84873530836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055953     Document Type: Article

References (68)

1. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, et al. (1996) Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. Journal of Applied Physiology 81: 355-361.
2. Olfert IM, Howlett RA, Tang K, Dalton ND, Gu Y, et al. (2009) Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. The Journal of Physiology 587: 1755.
3. Roudier E, Gineste C, Wazna A, Dehghan K, Desplanches D, et al. (2010) Angio-adaptation in unloaded skeletal muscle: new insights into an early and muscle type-specific dynamic process. The Journal of Physiology 588: 4579-4591.
4. Olfert IM, Birot O, (2011) Importance of Anti-angiogenic Factors in the Regulation of Skeletal Muscle Angiogenesis. Microcirculation 18: 316-330.
5. Jack L, (2000) The functions of thrombospondin-1 and-2. Current Opinion in Cell Biology 12: 634-640.
6. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, et al. (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nature medicine 6: 41-48.
7. Lange-Asschenfeldt B, Weninger W, Velasco P, Kyriakides TR, von Andrian UH, et al. (2002) Increased and prolonged inflammation and angiogenesis in delayed-type hypersensitivity reactions elicited in the skin of thrombospondin-2-deficient mice. Blood 99: 538-545.
8. Varma V, Yao-Borengasser A, Bodles AM, Rasouli N, Phanavanh B, et al. (2008) Thrombospondin-1 Is an Adipokine Associated With Obesity, Adipose Inflammation, and Insulin Resistance. Diabetes 57: 432-439.
9. Ridnour LA, Isenberg JS, Espey MG, Thomas DD, Roberts DD, et al. (2005) Nitric oxide regulates angiogenesis through a functional switch involving thrombospondin-1. Proceedings of the National Academy of Sciences of the United States of America 102: 13147-13152.
10. Kvansakul M, Adams JC, Hohenester E, (2004) Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J 23: 1223-1233.
11. Chen H, Herndon ME, Lawler J, (2000) The cell biology of thrombospondin-1. Matrix Biology 19: 597-614.
12. Febbraio M, Hajjar DP, Silverstein RL, (2001) CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. Journal of Clinical Investigation 108: 785-792.
13. Primo L, Ferrandi C, Roca C, Marchiò S, di Blasio L, et al. (2005) Identification of CD36 molecular features required for its in vitro angiostatic activity. The FASEB journal 19: 1713-1715.
14. Ren B, Yee KO, Lawler J, Khosravi-Far R, (2006) Regulation of tumor angiogenesis by thrombospondin-1. Biochimica et Biophysica Acta (BBA)- Reviews on Cancer 1765: 178-188.
15. Hoekstra R, de Vos FYFL, Eskens FALM, Gietema JA, van der Gaast A, et al. (2005) Phase I Safety, Pharmacokinetic, and Pharmacodynamic Study of the Thrombospondin-1-Mimetic Angiogenesis Inhibitor ABT-510 in Patients With Advanced Cancer. Journal of Clinical Oncology 23: 5188-5197.
16. Reiher FK, Volpert OV, Jimenez B, Crawford SE, Dinney CP, et al. (2002) Inhibition of tumor growth by systemic treatment with thrombospondin-1 peptide mimetics. International Journal of Cancer 98: 682-689.
17. Rusk A, McKeegan E, Haviv F, Majest S, Henkin J, et al. (2006) Preclinical Evaluation of Antiangiogenic Thrombospondin-1 Peptide Mimetics, ABT-526 and ABT-510, in Companion Dogs with Naturally Occurring Cancers. Clinical Cancer Research 12: 7444-7455.
18. Olfert IM, Breen EC, Gavin TP, Wagner PD, (2006) Temporal thrombospondin-1 mRNA response in skeletal muscle exposed to acute and chronic exercise. Growth Factors 24: 253-259.
19. Olfert IM (2012) Unpublished Data.
20. Frazier EP, Isenberg JS, Shiva S, Zhao L, Schlesinger P, et al. (2011) Age-dependent regulation of skeletal muscle mitochondria by the thrombospondin-1 receptor CD47. Matrix Biology.
21. Dawson DW, Pearce SFA, Zhong R, Silverstein RL, Frazier WA, et al. (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. The Journal of cell biology 138: 707.
22. Haviv F, Bradley MF, Kalvin DM, Schneider AJ, Davidson DJ, et al. (2005) Thrombospondin-1 mimetic peptide inhibitors of angiogenesis and tumor growth: design, synthesis, and optimization of pharmacokinetics and biological activities. Journal of medicinal chemistry 48: 2838-2846.
23. Anderson JC, Grammer JR, Wang W, Nabors LB, Henkin J, et al. (2007) ABT-510, a modified type 1 repeat peptide of thrombospondin, inhibits malignant glioma growth in vivo by inhibiting angiogenesis. Cancer biology & therapy 6: 454.
24. Greenaway J, Henkin J, Lawler J, Moorehead R, Petrik J, (2009) ABT-510 induces tumor cell apoptosis and inhibits ovarian tumor growth in an orthotopic, syngeneic model of epithelial ovarian cancer. Molecular cancer therapeutics 8: 64.
25. Rusk A, McKeegan E, Haviv F, Majest S, Henkin J, et al. (2006) Preclinical evaluation of antiangiogenic thrombospondin-1 peptide mimetics, ABT-526 and ABT-510, in companion dogs with naturally occurring cancers. Clinical cancer research 12: 7444.
26. Yap R, Veliceasa D, Emmenegger U, Kerbel RS, McKay LM, et al. (2005) Metronomic low-dose chemotherapy boosts CD95-dependent antiangiogenic effect of the thrombospondin peptide ABT-510: a complementation antiangiogenic strategy. Clinical cancer research 11: 6678.
27. Campbell NE, Greenaway J, Henkin J, Moorehead RA, Petrik J The Thrombospondin-1 Mimetic ABT-510 Increases the Uptake and Effectiveness of Cisplatin and Paclitaxel in a Mouse Model of Epithelial Ovarian Cancer. Neoplasia Press Inc.
28. Isenberg JS, Yu C, Roberts DD, (2008) Differential effects of ABT-510 and a CD36-binding peptide derived from the type 1 repeats of thrombospondin-1 on fatty acid uptake, nitric oxide signaling, and caspase activation in vascular cells. Biochemical Pharmacology 75: 875-882.
29. Hasina R, Martin LE, Kasza K, Jones CL, Jalil A, et al. (2009) ABT-510 is an effective chemopreventive agent in the mouse 4-nitroquinoline 1-oxide model of oral carcinogenesis. Cancer Prevention Research 2: 385.
30. Joyce D, Mulji G, Gutierrez L, Castellino F, (2006) Evaluation of the Thrombospondin-1 analogue ABT-510 in the APCMin/+ mouse intestinal adenoma model. Journal of Clinical Oncology 24: 13545.
31. Mrázková O, Grim M, Carlson BM, (1986) Enzymatic heterogeneity of the capillary bed of rat skeletal muscles. American Journal of Anatomy 177: 141-148.
32. Lojda Z, (1979) Studies on dipeptidyl(amino)peptidase IV (glycyl-proline naphthylamidase). Histochemistry 59: 153-166.
33. Malek MH, Olfert IM, (2009) Global deletion of thrombospondin 1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Experimental physiology 94: 749-760.
34. Roudier E, Gineste C, Wazna A, Dehghan K, Desplanches D, et al. (2010) Angio-adaptation in unloaded skeletal muscle: new insights into an early and muscle type-specific dynamic process. The Journal of Physiology 588: 4579.
35. Bornstein P, (2009) Thrombospondins function as regulators of angiogenesis. Journal of Cell Communication and Signaling 3: 189-200.
36. Lawler J, (2000) The functions of thrombospondin-1 and-2. Current opinion in cell biology 12: 634-640.
37. Zhang X, Lawler J, (2007) Thrombospondin-based antiangiogenic therapy. Microvascular research 74: 90-99.
38. Lawler J, Detmar M, (2004) Tumor progression: the effects of thrombospondin-1 and-2. The International Journal of Biochemistry & Cell Biology 36: 1038-1045.
39. Kivela R, Silvennoinen M, Lehti M, Jalava S, Vihko V, et al. (2008) Exercise-induced expression of angiogenic growth factors in skeletal muscle and in capillaries of healthy and diabetic mice. Cardiovascular Diabetology 7: 13.
40. Kivelä R, Silvennoinen M, Touvra A-M, Lehti TM, Kainulainen H, et al. (2006) Effects of experimental type 1 diabetes and exercise training on angiogenic gene expression and capillarization in skeletal muscle. The FASEB journal 20: 1570-1572.
41. Duscha BD, Kraus WE, Keteyian SJ, Sullivan MJ, Green HJ, et al. (1999) Capillary density of skeletal muscle: A contributing mechanism for exercise intolerance in class II-III chronic heart failure independent of other peripheral alterations. Journal of the American College of Cardiology 33: 1956-1963.
42. Greenaway J, Lawler J, Moorehead R, Bornstein P, Lamarre J, et al. (2007) Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). Journal of cellular physiology 210: 807-818.
43. Gupta K, Gupta P, Wild R, Ramakrishnan S, Hebbel R, (1999) Binding and displacement of vascular endothelial growth factor (VEGF) by thrombospondin: Effect on human microvascular endothelial cell proliferation and angiogenesis. Angiogenesis 3: 147-158.
44. Iruela-Arispe ML, Lombardo M, Krutzsch HC, Lawler J, Roberts DD, (1999) Inhibition of Angiogenesis by Thrombospondin-1 Is Mediated by 2 Independent Regions Within the Type 1 Repeats. Circulation 100: 1423-1431.
45. Rodríguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, et al. (2001) Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proceedings of the National Academy of Sciences of the United States of America 98: 12485.
46. Sun J, Hopkins BD, Tsujikawa K, Perruzzi C, Adini I, et al. (2009) Thrombospondin-1 modulates VEGF-A-mediated Akt signaling and capillary survival in the developing retina. American Journal of Physiology-Heart and Circulatory Physiology 296: H1344.
47. Simons M, (2012) An Inside View: VEGF Receptor Trafficking and Signaling. Physiology 27: 213-222.
48. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, et al. (2010) Thrombospondin-1 Inhibits VEGF Receptor-2 Signaling by Disrupting Its Association with CD47. Journal of Biological Chemistry 285: 38923-38932.
49. Zhang X, Kazerounian S, Duquette M, Perruzzi C, Nagy JA, et al. (2009) Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. The FASEB journal 23: 3368-3376.
50. Zhang X, Kazerounian S, Duquette M, Perruzzi C, Nagy JA, et al. (2009) Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. The FASEB journal 23: 3368.
51. Reiher FK, Volpert OV, Jimenez B, Crawford SE, Dinney CP, et al. (2002) Inhibition of tumor growth by systemic treatment with thrombospondin 1 peptide mimetics. International journal of cancer 98: 682-689.
52. Friedl P, Vischer P, Freyberg M, (2002) The role of thrombospondin-1 in apoptosis. Cellular and molecular life sciences 59: 1347-1357.
53. Guo N, Krutzsch HC, Inman JK, Roberts DD, (1997) Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer research 57: 1735.
54. Miao W-M, Lin Seng W, Duquette M, Lawler P, Laus C, et al. (2001) Thrombospondin-1 Type 1 Repeat Recombinant Proteins Inhibit Tumor Growth through Transforming Growth Factor-β-dependent and-independent Mechanisms. Cancer research 61: 7830-7839.
55. Nör J, Mitra RS, Sutorik MM, Mooney DJ, Castle VP, et al. (2000) Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. Journal of vascular research 37: 209-218.
56. Isenberg J, Frazier W, Roberts D, (2008) Thrombospondins: from structure to therapeutics: Thrombospondin-1: a physiological regulator of nitric oxide signaling. Cellular and Molecular Life Sciences CMLS 65: 728-742.
57. Isenberg JS, Hyodo F, Matsumoto KI, Romeo MJ, Abu-Asab M, et al. (2007) Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 109: 1945.
58. Isenberg JS, Ridnour LA, Perruccio EM, Espey MG, Wink DA, et al. (2005) Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 102: 13141.
59. Wintergerst ES, Jelk J, Rahner C, Asmis R, (2000) Apoptosis induced by oxidized low density lipoprotein in human monocyte-derived macrophages involves CD36 and activation of caspase-3. European Journal of Biochemistry 267: 6050-6059.
60. Meeson AP, Argilla M, Ko K, Witte L, Lang RA, (1999) VEGF deprivation-induced apoptosis is a component of programmed capillary regression. Development 126: 1407-1415.
61. Tang K, Breen EC, Gerber H-P, Ferrara NMA, Wagner PD, (2004) Capillary regression in vascular endothelial growth factor-deficient skeletal muscle. Physiological Genomics 18: 63-69.
62. Meeson A, Palmer M, Calfon M, Lang R, (1996) A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development 122: 3929-3938.
63. Dimmeler S, Zeiher AM, (2000) Endothelial Cell Apoptosis in Angiogenesis and Vessel Regression. Circulation research 87: 434-439.
64. Degens H, Alway SE, (2006) Control of muscle size during disuse, disease, and aging. International journal of sports medicine 27: 94-99.
65. Siu PM, Pistilli EE, Butler DC, Alway SE, (2005) Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. American Journal of Physiology- Cell Physiology 288: C338-C349.
66. dalla Libera L, Zennaro R, Sandri M, Ambrosio GB, Vescovo G, (1999) Apoptosis and atrophy in rat slow skeletal muscles in chronic heart failure. American Journal of Physiology- Cell Physiology 277: C982-C986.
67. Dupont-Versteegden EE, (2005) Apoptosis in muscle atrophy: Relevance to sarcopenia. Experimental Gerontology 40: 473-481.
68. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, et al. (1997) Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. American Journal of Physiology- Cell Physiology 273: C579-C587.