Targeting the endothelial progenitor cell surface proteome to identify novel mechanisms that mediate angiogenic efficacy in a rodent model of vascular disease

Physiological Genomics

Volumn 45, Issue 21, 2013, Pages 999-1011

  Kaczorowski, Catherine C ^a,b   Stodola, Timothy J ^a   Hoffmann, Brian R ^a   Prisco, Anthony R ^a   Liu, Pengyuan Y ^a   Didier, Daniela N ^a   Karcher, Jamie R ^a   Liang, Mingyu ^a   Jacob, Howard J ^a   Greene, Andrew S ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Angiogenesis; Endothelial progenitor cell; Genome wide transcript profiling; Proteomics; Rat model of vascular disease; RNA sequencing

Indexed keywords

CD244 ANTIGEN; CELL SURFACE PROTEIN; ENDOTHELIAL CELL GROWTH FACTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN FC FRAGMENT; PROTEOME; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; BONE MARROW CELL; CELL DEATH; CELL SURFACE; CELL THERAPY; CHEMICAL LABELING; CONTROLLED STUDY; DRUG EFFICACY; ELECTROSTIMULATION; ENDOTHELIAL PROGENITOR CELL; GENE SEQUENCE; GENETIC TRANSCRIPTION; MASS SPECTROMETRY; NATURAL KILLER CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROBABILITY; PROTEIN TARGETING; REGENERATIVE MEDICINE; RNA SEQUENCE; SCREENING; VASCULAR DISEASE;

ANGIOGENESIS; ENDOTHELIAL PROGENITOR CELL; GENOME-WIDE TRANSCRIPT PROFILING; PROTEOMICS; RAT MODEL OF VASCULAR DISEASE; RNA SEQUENCING;

ANIMALS; ANTIGENS, CD34; CELLS, CULTURED; ELECTRIC STIMULATION; ENDOTHELIAL CELLS; FLOW CYTOMETRY; HUMANS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEOME; RATS; RATS, INBRED BN; RATS, INBRED DAHL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSCRIPTOME; VASCULAR DISEASES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84887110240     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00097.2013     Document Type: Article

References (68)

1. Abe M, O'Connor P, Kaldunski M, Liang M, Roman RJ, Cowley AW Jr. Effect of sodium delivery on superoxide and nitric oxide in the medullary thick ascending limb. Am J Physiol Renal Physiol 291: F350-F357, 2006.
2. Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, Mangion J, Roberton-Lowe C, Marshall AJ, Petretto E, Hodges MD, Bhangal G, Patel SG, Sheehan-Rooney K, Duda M, Cook PR, Evans DJ, Domin J, Flint J, Boyle JJ, Pusey CD, Cook HT. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439: 851-855, 2006.
3. Amaral SL, Linderman JR, Morse MM, Greene AS. Angiogenesis induced by electrical stimulation is mediated by angiotensin II and VEGF. Microcirculation 8: 57-67, 2001.
4. Amaral SL, Roman RJ, Greene AS. Renin gene transfer restores angiogenesis and vascular endothelial growth factor expression in Dahl S rats. Hypertension 37: 386-390, 2001.
5. Asahara T, Kawamoto A, Masuda H. Concise review: Circulating endothelial progenitor cells for vascular medicine. Stem Cells 29: 1650-1655, 2011.
6. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997.
7. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289-300, 1995.
8. Boegehold MA, Kotchen TA. Arteriolar network morphology in gracilis muscle of rats with salt-induced hypertension. Microvasc Res 40: 169-178, 1990.
9. Boles NC, Lin KK, Lukov GL, Bowman TV, Baldridge MT, Goodell MA. CD48 on hematopoietic progenitors regulates stem cells and suppresses tumor formation. Blood 118: 80-87, 2011.
10. Brown DR, Calpe S, Keszei M, Wang N, McArdel S, Terhorst C, Sharpe AH. Cutting edge: an NK cell-independent role for Slamf4 in controlling humoral autoimmunity. J Immunol 187: 21-25, 2011.
11. Caiado F, Dias S. Endothelial progenitor cells and integrins: adhesive needs. Fibrogenesis Tissue Repair 5: 4, 2012.
12. Chen II, Prewitt RL, Dowell RF. Microvascular rarefaction in spontaneously hypertensive rat cremaster muscle. Am J Physiol Heart Circ Physiol 241: H306-H310, 1981.
13. Cheung NK, Sowers R, Vickers AJ, Cheung IY, Kushner BH, Gorlick R. FCGR2A polymorphism is correlated with clinical outcome after immunotherapy of neuroblastoma with anti-GD2 antibody and granulo-cyte macrophage colony-stimulating factor. J Clin Oncol 24: 2885-2890, 2006.
14. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, Robertson AJ, Perkins AC, Bruce SJ, Lee CC, Ranade SS, Peckham HE, Manning JM, McKernan KJ, Grimmond SM. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Meth 5: 613-619, 2008.
15. Cowley AW Jr, Roman RJ, Kaldunski ML, Dumas P, Dickhout JG, Greene AS, Jacob HJ. Brown Norway chromosome 13 confers protection from high salt to consomic Dahl S rat. Hypertension 37: 456-461, 2001.
16. Crick FH. On protein synthesis. Symp Soc Exp Biol 12: 138-163, 1958.
17. de Resende MM, Amaral SL, Moreno C, Greene AS. Congenic strains reveal the effect of the renin gene on skeletal muscle angiogenesis induced by electrical stimulation. Physiol Genomics 33: 33-40, 2008.
18. de Resende MM, Stodola TJ, Greene AS. Role of the renin angiotensin system on bone marrow-derived stem cell function and its impact on skeletal muscle angiogenesis. Physiol Genomics 42: 437-444, 2010.
19. Dimmeler S, Losordo D. Stem cells review series: an introduction. Circ Res 109: 907-909, 2011.
20. Dwinell MR, Worthey EA, Shimoyama M, Bakir-Gungor B, DePons J, Laulederkind S, Lowry T, Nigram R, Petri V, Smith J, Stoddard A, Twigger SN, Jacob HJ, Team RGD. The Rat Genome Database 2009: variation, ontologies and pathways. Nucl Acids Res 37: D744-D749, 2009.
21. Emanueli C, Salis MB, Stacca T, Gaspa L, Chao J, Chao L, Piana A, Madeddu P. Rescue of impaired angiogenesis in spontaneously hypertensive rats by intramuscular human tissue kallikrein gene transfer. Hypertension 38: 136-141, 2001.
22. Garber M, Grabherr MG, Guttman M, Trapnell C. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Meth 8: 469-477, 2011.
23. Gundry RL, Raginski K, Tarasova Y, Tchernyshyov I, Bausch-Fluck D, Elliott ST, Boheler KR, Van Eyk JE, Wollscheid B. The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Mol Cell Proteom 8: 2555-2569, 2009.
24. Guryev V, Saar K, Adamovic T, Verheul M, van Heesch SA, Cook S, Pravenec M, Aitman T, Jacob H, Shull JD, Hubner N, Cuppen E. Distribution and functional impact of DNA copy number variation in the rat. Nat Genet 40: 538-545, 2008.
25. Halligan BD, Geiger JF, Vallejos AK, Greene AS, Twigger SN. Low cost, scalable proteomics data analysis using Amazon's cloud computing services and open source search algorithms. J Proteome Res 8: 3148-3153, 2009.
26. Halligan BD, Greene AS. Visualize: a free and open source multifunction tool for proteomics data analysis. Proteomics 11: 1058-1063, 2011.
27. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348: 593-600, 2003.
28. Hristov M, Weber C. Endothelial progenitor cells in vascular repair and remodeling. Pharm Res 58: 148-151, 2008.
29. Iwasaki H, Kawamoto A, Ishikawa M, Oyamada A, Nakamori S, Nishimura H, Sadamoto K, Horii M, Matsumoto T, Murasawa S, Shibata T, Suehiro S, Asahara T. Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and car-diomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 113: 1311-1325, 2006.
30. Jarajapu YP, Grant MB. The promise of cell-based therapies for diabetic complications: challenges and solutions. Circ Res 106: 854-869, 2010.
31. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 97: 3422-3427, 2000.
32. Kanno S, Oda N, Abe M, Saito S, Hori K, Handa Y, Tabayashi K, Sato Y. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 99: 2682-2687, 1999.
33. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103: 634-637, 2001.
34. Kawamoto A, Iwasaki H, Kusano K, Murayama T, Oyamada A, Silver M, Hulbert C, Gavin M, Hanley A, Ma H, Kearney M, Zak V, Asahara T, Losordo DW. CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation 114: 2163-2169, 2006.
35. Kawamoto A, Katayama M, Handa N, Kinoshita M, Takano H, Horii M, Sadamoto K, Yokoyama A, Yamanaka T, Onodera R, Kuroda A, Baba R, Kaneko Y, Tsukie T, Kurimoto Y, Okada Y, Kihara Y, Morioka S, Fukushima M, Asahara T. Intramuscular transplantation of G-CSF-mobilized CD34(+) cells in patients with critical limb ischemia: a phase I/IIa, multicenter, single-blinded, dose-escalation clinical trial. Stem Cells 27: 2857-2864, 2009.
36. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7: 430-436, 2001.
37. Linderman JR, Kloehn MR, Greene AS. Development of an implantable muscle stimulator: measurement of stimulated angiogenesis and poststimulus vessel regression. Microcirculation 7: 119-128, 2000.
38. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523-536, 2008.
39. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld AJ. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53: 195-199, 2004.
40. McKinney C, Fanciulli M, Merriman ME, Phipps-Green A, Alizadeh BZ, Koeleman BP, Dalbeth N, Gow PJ, Harrison AA, Highton J, Jones PB, Stamp LK, Steer S, Barrera P, Coenen MJ, Franke B, van Riel PL, Vyse TJ, Aitman TJ, Radstake TR, Merriman TR. Association of variation in Fcgamma receptor 3B gene copy number with rheumatoid arthritis in Caucasian samples. Ann Rheum Dis 69: 1711-1716, 2010.
41. Messmer B, Eissmann P, Stark S, Watzl C. CD48 stimulation by 2B4 (CD244)-expressing targets activates human NK cells. J Immunol 176: 4646-4650, 2006.
42. Morris DL, Roberts AL, Witherden AS, Tarzi R, Barros P, Whittaker JC, Cook TH, Aitman TJ, Vyse TJ. Evidence for both copy number and allelic (NA1/NA2) risk at the FCGR3B locus in systemic lupus erythematosus. Eur J Hum Genet 18: 1027-1031, 2010.
43. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Meth 5: 621-628, 2008.
44. Murohara T, Ikeda H, Duan J, Shintani S, Sasaki K, Eguchi H, Onitsuka I, Matsui K, Imaizumi T. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 105: 1527-1536, 2000.
45. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349, 2008.
46. Niederer HA, Willcocks LC, Rayner TF, Yang W, Lau YL, Williams TN, Scott JA, Urban BC, Peshu N, Dunstan SJ, Hien TT, Phu NH, Padyukov L, Gunnarsson I, Svenungsson E, Savage CO, Watts RA, Lyons PA, Clayton DG, Smith KG. Copy number, linkage disequilibrium and disease association in the FCGR locus. Hum Mol Genet 19: 3282-3294, 2010.
47. Ota Y, Kawaguchi Y, Takagi K, Tochimoto A, Kawamoto M, Kat-sumata Y, Gono T, Masuda I, Ikari K, Momohara S, Yamanaka H. Single nucleotide polymorphisms of CD244 gene predispose to renal and neuropsychiatric manifestations with systemic lupus erythematosus. Mod Rheumatol 20: 427-431, 2010.
48. Parker SJ. The Effect of Bone Marrow Derived Stem Cell Transfer on Cardiac Structure and Function During Hypertensive Heart Disease in the Salt-Sensitive Rat (PhD thesis). Milwaukee, WI: Medical College of Wisconsin, 2011.
49. Parker SJ, Didier DN, Karcher JR, Stodola TJ, Endres B, Greene AS. Bone marrow mononuclear cells induce beneficial remodeling and reduce diastolic dysfunction in the left ventricle of hypertensive SS/MCWi rats. Physiol Genomics 44: 925-933, 2012.
50. Petersen MC, Munzenmaier DH, Greene AS. Angiotensin II infusion restores stimulated angiogenesis in the skeletal muscle of rats on a high-salt diet. Am J Physiol Heart Circ Physiol 291: H114-H120, 2006.
51. Phillips NE, Parker DC. Cross-linking of B lymphocyte Fc gamma receptors and membrane immunoglobulin inhibits anti-immunoglobulin-induced blastogenesis. J Immunol 132: 627-632, 1984.
52. Redondo S, Gonzalez-Rocafort A, Navarro-Dorado J, Ramajo M, Hristov M, Gordillo-Moscoso A, Reguillo F, Carnero M, Martinez-Gonzalez J, Rodriguez E, Weber C, Tejerina T. Decreased pre-surgical CD34+/CD144+ cell number in patients undergoing coronary artery bypass grafting compared to coronary artery disease-free valvular patients. J Card Surg 7: 2, 2012.
53. Schiess R, Mueller LN, Schmidt A, Mueller M, Wollscheid B, Aeber-sold R. Analysis of cell surface proteome changes via label-free, quantitative mass spectrometry. Mol Cell Proteom 8: 624-638, 2009.
54. Shaffer RG, Greene S, Arshi A, Supple G, Bantly A, Moore JS, Mohler ER 3rd. Flow cytometric measurement of circulating endothelial cells: the effect of age and peripheral arterial disease on baseline levels of mature and progenitor populations. Cytometry B Clin Cytome 70: 56-62, 2006.
55. Shantsila E, Watson T, Lip GY. Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol 49: 741-752, 2007.
56. Stodola TJ, de Resende MM, Sarkis AB, Didier DN, Jacob HJ, Huebner N, Hummel O, Saar K, Moreno C, Greene AS. Characterization of the genomic structure and function of regions influencing renin and angiogenesis in the SS rat. Physiol Genomics 43: 808-817, 2011.
57. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 379: 346-349, 1996.
58. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106: 2781-2786, 2002.
59. Thomas RA, Pietrzak DC, Scicchitano MS, Thomas HC, McFarland DC, Frazier KS. Detection and characterization of circulating endothelial progenitor cells in normal rat blood. J Pharmacol Toxicol Meth 60: 263-274, 2009.
60. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111, 2009.
61. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protocols 7: 562-578, 2012.
62. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quan-tification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515, 2010.
63. van der Pol W, van de Winkel JG. IgG receptor polymorphisms: risk factors for disease. Immunogenetics 48: 222-232, 1998.
64. van der Straaten HM, Fijnheer R, Nieuwenhuis HK, van de Winkel JG, Verdonck LF. The FcgammaRIIa-polymorphic site as a potential target for acute graft-versus-host disease in allogeneic stem cell transplantation. Biol Blood Marrow Transplant 11: 206-212, 2005.
65. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7, 2001.
66. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243, 2008.
67. Wollscheid B, Bausch-Fluck D, Henderson C, O'Brien R, Bibel M, Schiess R, Aebersold R, Watts JD. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotech-nol 27: 378-386, 2009.
68. Yamamoto K, Kondo T, Suzuki S, Izawa H, Kobayashi M, Emi N, Komori K, Naoe T, Takamatsu J, Murohara T. Molecular evaluation of endothelial progenitor cells in patients with ischemic limbs: therapeutic effect by stem cell transplantation. Arterioscler Thromb Vasc Biol 24: e192-e196, 2004.