Levels of soluble platelet endothelial cell adhesion molecule-1 and P-selectin are decreased in children with autism spectrum disorder

Biological Psychiatry

Volumn 72, Issue 12, 2012, Pages 1020-1025

  Onore, Charity E ^a,b   Nordahl, Christine Wu ^b,c   Young, Gregory S ^b,c   Van De Water, Judy A ^b,c   Rogers, Sally J ^b,c   Ashwood, Paul ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adhesion; autism; CD31; CD62 P; P Selectin; PECAM 1

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; L SELECTIN; PADGEM PROTEIN; PLATELET ENDOTHELIAL ADHESION MOLECULE 1; UNCLASSIFIED DRUG; VASCULAR ADHESION MOLECULE 1;

ARTICLE; AUTISM; BEHAVIOR; BRAIN GROWTH; CELL MIGRATION; CHILD; CLINICAL ARTICLE; FEMALE; HEAD CIRCUMFERENCE; HUMAN; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL;

ANTIGENS, CD31; BRAIN; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; DATA INTERPRETATION, STATISTICAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEAD; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; L-SELECTIN; MALE; P-SELECTIN; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84869082809     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.05.004     Document Type: Article

References (83)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 4th edition, text revision 2000 American Psychiatric Publishing Arlington, VA
2. Morbidity and Mortality Weekly Report Prevalence of autism spectrum disorders - Autism and Developmental Disabilities Monitoring Network, United States, 2006 MMWR Surveill Summ 58 2009 1 20
3. P. Ashwood, S. Wills, J. Van de Water The immune response in autism: A new frontier for autism research J Leukoc Biol 80 2006 1 15
4. A.M. Enstrom, J.A. Van de Water, P. Ashwood Autoimmunity in autism Curr Opin Investig Drugs 10 2009 463 473
5. P.H. Patterson Immune involvement in schizophrenia and autism: Etiology, pathology and animal models Behav Brain Res 204 2009 313 321
6. M. Careaga, J. Van de Water, P. Ashwood Immune dysfunction in autism: A pathway to treatment Neurotherapeutics 7 2010 283 292
7. D.L. Vargas, C. Nascimbene, C. Krishnan, A.W. Zimmerman, C.A. Pardo Neuroglial activation and neuroinflammation in the brain of patients with autism Ann Neurol 57 2005 67 81
8. P. Ashwood, A. Enstrom, P. Krakowiak, I. Hertz-Picciotto, R.L. Hansen, L.A. Croen Decreased transforming growth factor beta1 in autism: A potential link between immune dysregulation and impairment in clinical behavioral outcomes J Neuroimmunol 204 2008 149 153
9. P. Ashwood, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, I. Pessah, J. Van de Water Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome Brain Behav Immun 25 2011 40 45
10. P. Ashwood, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, I.N. Pessah, J. Van de Water Associations of impaired behaviors with elevated plasma chemokines in autism spectrum disorders J Neuroimmunol 232 2011 196 199
11. J. Croonenberghs, A. Wauters, K. Devreese, R. Verkerk, S. Scharpe, E. Bosmans Increased serum albumin, gamma globulin, immunoglobulin IgG, and IgG2 and IgG4 in autism Psychol Med 32 2002 1457 1463
12. L. Heuer, P. Ashwood, J. Schauer, P. Goines, P. Krakowiak, I. Hertz-Picciotto Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms Autism Res 1 2008 275 283
13. A. Enstrom, P. Krakowiak, C. Onore, I.N. Pessah, I. Hertz-Picciotto, R.L. Hansen Increased IgG4 levels in children with autism disorder Brain Behav Immun 23 2009 389 395
14. R.P. Warren, L.J. Yonk, R.A. Burger, P. Cole, J.D. Odell, W.L. Warren Deficiency of suppressor-inducer (CD4+CD45RA+) T cells in autism Immunol Invest 19 1990 245 251
15. L.J. Yonk, R.P. Warren, R.A. Burger, P. Cole, J.D. Odell, W.L. Warren CD4+ helper T cell depression in autism Immunol Lett 25 1990 341 345
16. D.R. Denney, B.W. Frei, G.R. Gaffney Lymphocyte subsets and interleukin-2 receptors in autistic children J Autism Dev Disord 26 1996 87 97
17. S. Gupta, S. Aggarwal, B. Rashanravan, T. Lee Th1- and Th2-like cytokines in CD4+ and CD8+ T cells in autism J Neuroimmunol 85 1998 106 109
18. P. Ashwood, A. Anthony, A.A. Pellicer, F. Torrente, J.A. Walker-Smith, A.J. Wakefield Intestinal lymphocyte populations in children with regressive autism: Evidence for extensive mucosal immunopathology J Clin Immunol 23 2003 504 517
19. P. Ashwood, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, I.N. Pessah, J. Van de Water Altered T cell responses in children with autism Brain Behav Immun 25 2011 840 849
20. R.P. Warren, A. Foster, N.C. Margaretten Reduced natural killer cell activity in autism J Am Acad Child Adolesc Psychiatry 26 1987 333 335
21. A. Vojdani, E. Mumper, D. Granpeesheh, L. Mielke, D. Traver, K. Bock Low natural killer cell cytotoxic activity in autism: The role of glutathione, IL-2 and IL-15 J Neuroimmunol 205 2008 148 154
22. A.M. Enstrom, L. Lit, C.E. Onore, J.P. Gregg, R.L. Hansen, I.N. Pessah Altered gene expression and function of peripheral blood natural killer cells in children with autism Brain Behav Immun 23 2009 124 133
23. H. Jyonouchi, S. Sun, H. Le Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression J Neuroimmunol 120 2001 170 179
24. T.L. Sweeten, D.J. Posey, C.J. McDougle High blood monocyte counts and neopterin levels in children with autistic disorder Am J Psychiatry 160 2003 1691 1693
25. A.M. Enstrom, C.E. Onore, J.A. Van de Water, P. Ashwood Differential monocyte responses to TLR ligands in children with autism spectrum disorders Brain Behav Immun 24 2010 64 71
26. D. Braunschweig, P. Ashwood, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, L.A. Croen Autism: Maternally derived antibodies specific for fetal brain proteins Neurotoxicology 29 2008 226 231
27. L.A. Martin, P. Ashwood, D. Braunschweig, M. Cabanlit, J. Van de Water, D.G. Amaral Stereotypies and hyperactivity in rhesus monkeys exposed to IgG from mothers of children with autism Brain Behav Immun 22 2008 806 816
28. H.S. Singer, C. Morris, C. Gause, M. Pollard, A.W. Zimmerman, M. Pletnikov Prenatal exposure to antibodies from mothers of children with autism produces neurobehavioral alterations: A pregnant dam mouse model J Neuroimmunol 211 2009 39 48
29. S. Wills, M. Cabanlit, J. Bennett, P. Ashwood, D.G. Amaral, J. Van de Water Detection of autoantibodies to neural cells of the cerebellum in the plasma of subjects with autism spectrum disorders Brain Behav Immun 23 2009 64 74
30. V.K. Singh Plasma increase of interleukin-12 and interferon-gamma Pathological significance in autism J Neuroimmunol 66 1996 143 145
31. K. Okada, K. Hashimoto, Y. Iwata, K. Nakamura, M. Tsujii, K.J. Tsuchiya Decreased serum levels of transforming growth factor-beta1 in patients with autism Prog Neuropsychopharmacol Biol Psychiatry 31 2007 187 190
32. L.A. Croen, P. Goines, D. Braunschweig, R. Yolken, C.K. Yoshida, J.K. Grether Brain-derived neurotrophic factor and autism: Maternal and infant peripheral blood levels in the Early Markers for Autism (EMA) Study Autism Res 1 2008 130 137
33. E.L. Grigorenko, S.S. Han, C.M. Yrigollen, L. Leng, Y. Mizue, G.M. Anderson Macrophage migration inhibitory factor and autism spectrum disorders Pediatrics 122 2008 e438 e445
34. J. Croonenberghs, E. Bosmans, D. Deboutte, G. Kenis, M. Maes Activation of the inflammatory response system in autism Neuropsychobiology 45 2002 1 6
35. H. Jyonouchi, L. Geng, A. Ruby, C. Reddy, B. Zimmerman-Bier Evaluation of an association between gastrointestinal symptoms and cytokine production against common dietary proteins in children with autism spectrum disorders J Pediatr 146 2005 605 610
36. C.A. Molloy, A.L. Morrow, J. Meinzen-Derr, K. Schleifer, K. Dienger, P. Manning-Courtney Elevated cytokine levels in children with autism spectrum disorder J Neuroimmunol 172 2006 198 205
37. C. Onore, A. Enstrom, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, J. Van de Water Decreased cellular IL-23 but not IL-17 production in children with autism spectrum disorders J Neuroimmunol 216 2009 126 129
38. X. Li, A. Chauhan, A.M. Sheikh, S. Patil, V. Chauhan, X.M. Li Elevated immune response in the brain of autistic patients J Neuroimmunol 207 2009 111 116
39. A.W. Zimmerman, H. Jyonouchi, A.M. Comi, S.L. Connors, S. Milstien, A. Varsou Cerebrospinal fluid and serum markers of inflammation in autism Pediatr Neurol 33 2005 195 201
40. J.L. Baron, J.A. Madri, N.H. Ruddle, G. Hashim, C.A. Janeway Jr Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma J Exp Med 177 1993 57 68
41. K. Ley, C. Laudanna, M.I. Cybulsky, S. Nourshargh Getting to the site of inflammation: The leukocyte adhesion cascade updated Nat Rev Immunol 7 2007 678 689
42. M.K. Sharief, M.A. Noori, M. Ciardi, A. Cirelli, E.J. Thompson Increased levels of circulating ICAM-1 in serum and cerebrospinal fluid of patients with active multiple sclerosis Correlation with TNF-alpha and blood-brain barrier damage J Neuroimmunol 43 1993 15 21
43. J. Losy, A. Niezgoda, M. Wender Increased serum levels of soluble PECAM-1 in multiple sclerosis patients with brain gadolinium-enhancing lesions J Neuroimmunol 99 1999 169 172
44. K.J. Tsuchiya, K. Hashimoto, Y. Iwata, M. Tsujii, Y. Sekine, G. Sugihara Decreased serum levels of platelet-endothelial adhesion molecule (PECAM-1) in subjects with high-functioning autism: A negative correlation with head circumference at birth Biol Psychiatry 62 2007 1056 1058
45. Y. Iwata, K.J. Tsuchiya, S. Mikawa, K. Nakamura, Y. Takai, S. Suda Serum levels of P-selectin in men with high-functioning autism Br J Psychiatry 193 2008 338 339
46. C. Lord, S. Risi, L. Lambrecht, E.H. Cook Jr, B.L. Leventhal, P.C. DiLavore The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism J Autism Dev Disord 30 2000 205 223
47. C. Lord, M. Rutter, A. Le Couteur Autism Diagnostic Interview - Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders J Autism Dev Disord 24 1994 659 685
48. S.K. Berument, M. Rutter, C. Lord, A. Pickles, A. Bailey Autism screening questionnaire: Diagnostic validity Br J Psychiatry 175 1999 444 451
49. K.J. Rothman No adjustments are needed for multiple comparisons Epidemiology 1 1990 43 46
50. M. Schwartz, J. Kipnis A conceptual revolution in the relationships between the brain and immunity Brain Behav Immun 25 2011 817 819
51. J. Kipnis, H. Cohen, M. Cardon, Y. Ziv, M. Schwartz T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions Proc Natl Acad Sci U S A 101 2004 8180 8185
52. Y. Ziv, N. Ron, O. Butovsky, G. Landa, E. Sudai, N. Greenberg Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood Nat Neurosci 9 2006 268 275
53. N.C. Derecki, K.M. Quinnies, J. Kipnis Alternatively activated myeloid (M2) cells enhance cognitive function in immune compromised mice Brain Behav Immun 25 2011 379 385
54. N.C. Derecki, A.N. Cardani, C.H. Yang, K.M. Quinnies, A. Crihfield, K.R. Lynch Regulation of learning and memory by meningeal immunity: A key role for IL-4 J Exp Med 207 2010 1067 1080
55. Y. Ziv, A. Finkelstein, Y. Geffen, J. Kipnis, I. Smirnov, S. Shpilman A novel immune-based therapy for stroke induces neuroprotection and supports neurogenesis Stroke 38 2007 774 782
56. M. Schwartz, G. Moalem, R. Leibowitz-Amit, I.R. Cohen Innate and adaptive immune responses can be beneficial for CNS repair Trends Neurosci 22 1999 295 299
57. D.R. Beers, J.S. Henkel, W. Zhao, J. Wang, S.H. Appel CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS Proc Natl Acad Sci U S A 105 2008 15558 15563
58. I.M. Chiu, A. Chen, Y. Zheng, B. Kosaras, S.A. Tsiftsoglou, T.K. Vartanian T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS Proc Natl Acad Sci U S A 105 2008 17913 17918
59. L.K. Curran, C.J. Newschaffer, L.C. Lee, S.O. Crawford, M.V. Johnston, A.W. Zimmerman Behaviors associated with fever in children with autism spectrum disorders Pediatrics 120 2007 e1386 e1392
60. A.R. Torres Is fever suppression involved in the etiology of autism and neurodevelopmental disorders? BMC Pediatr 3 2003 9
61. Y.M.Y. Han, W.W.M. Leung, C.K. Wong, J.M.K. Lam, M.C. Cheung, A.S. Chan Lymphocyte subset alterations related to executive function deficits and repetitive stereotyped behavior in autism Res Autism Spect Dis 5 2011 486 494
62. P.E. Stenberg, R.P. McEver, M.A. Shuman, Y.V. Jacques, D.F. Bainton A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation J Cell Biol 101 1985 880 886
63. R. Bonfanti, B.C. Furie, B. Furie, D.D. Wagner PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells Blood 73 1989 1109 1112
64. R.P. McEver, R.D. Cummings Perspectives series: Cell adhesion in vascular biology Role of PSGL-1 binding to selectins in leukocyte recruitment J Clin Invest 100 1997 485 491
65. P.C. Burger, D.D. Wagner Platelet P-selectin facilitates atherosclerotic lesion development Blood 101 2003 2661 2666
66. A.D. Michelson, M.R. Barnard, H.B. Hechtman, H. MacGregor, R.J. Connolly, J. Loscalzo In vivo tracking of platelets: Circulating degranulated platelets rapidly lose surface P-selectin but continue to circulate and function Proc Natl Acad Sci U S A 93 1996 11877 11882
67. P.J. Newman, D.K. Newman Signal transduction pathways mediated by PECAM-1: New roles for an old molecule in platelet and vascular cell biology Arterioscler Thromb Vasc Biol 23 2003 953 964
68. W.A. Muller, S.A. Weigl, X. Deng, D.M. Phillips PECAM-1 is required for transendothelial migration of leukocytes J Exp Med 178 1993 449 460
69. A. Goldberger, K.A. Middleton, J.A. Oliver, C. Paddock, H.C. Yan, H.M. DeLisser Biosynthesis and processing of the cell adhesion molecule PECAM-1 includes production of a soluble form J Biol Chem 269 1994 17183 17191
70. N. Ilan, A. Mohsenin, L. Cheung, J.A. Madri PECAM-1 shedding during apoptosis generates a membrane-anchored truncated molecule with unique signaling characteristics FASEB J 15 2001 362 372
71. F. Liao, J. Ali, T. Greene, W.A. Muller Soluble domain 1 of platelet-endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo J Exp Med 185 1997 1349 1357
72. Z. Qing, M. Sandor, Z. Radvany, D. Sewell, A. Falus, D. Potthoff Inhibition of antigen-specific T cell trafficking into the central nervous system via blocking PECAM1/CD31 molecule J Neuropathol Exp Neurol 60 2001 798 807
73. L. Piccio, B. Rossi, E. Scarpini, C. Laudanna, C. Giagulli, A.C. Issekutz Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: Critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors J Immunol 168 2002 1940 1949
74. J. Kisucka, A.K. Chauhan, B.Q. Zhao, I.S. Patten, A. Yesilaltay, M. Krieger Elevated levels of soluble P-selectin in mice alter blood-brain barrier function, exacerbate stroke, and promote atherosclerosis Blood 113 2009 6015 6022
75. H.M. DeLisser, P.J. Newman, S.M. Albelda Molecular and functional aspects of PECAM-1/CD31 Immunol Today 15 1994 490 495
76. L.A. Schimmenti, H.C. Yan, J.A. Madri, S.M. Albelda Platelet endothelial cell adhesion molecule, PECAM-1, modulates cell migration J Cell Physiol 153 1992 417 428
77. E.K. Reinke, J. Lee, A. Zozulya, J. Karman, W.A. Muller, M. Sandor Short-term sPECAM-Fc treatment ameliorates EAE while chronic use hastens onset of symptoms J Neuroimmunol 186 2007 86 93
78. D. Graesser, A. Solowiej, M. Bruckner, E. Osterweil, A. Juedes, S. Davis Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice J Clin Invest 109 2002 383 392
79. Y. Persidsky, M. Stins, D. Way, M.H. Witte, M. Weinand, K.S. Kim A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis J Immunol 158 1997 3499 3510
80. B. Wispelwey, A.J. Lesse, E.J. Hansen, W.M. Scheld Haemophilus influenzae lipopolysaccharide-induced blood brain barrier permeability during experimental meningitis in the rat J Clin Invest 82 1988 1339 1346
81. R. Wilkinson, A.B. Lyons, D. Roberts, M.X. Wong, P.A. Bartley, D.E. Jackson Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease Blood 100 2002 184 193
82. G.S. Duncan, D.P. Andrew, H. Takimoto, S.A. Kaufman, H. Yoshida, J. Spellberg Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions J Immunol 162 1999 3022 3030
83. S. Mahooti, D. Graesser, S. Patil, P. Newman, G. Duncan, T. Mak PECAM-1 (CD31) expression modulates bleeding time in vivo Am J Pathol 157 2000 75 81