The effects of human immunoglobulin G on enhancing tissue protection and neurobehavioral recovery after traumatic cervical spinal cord injury are mediated through the neurovascular unit.


Journal

Journal of neuroinflammation
ISSN: 1742-2094
Titre abrégé: J Neuroinflammation
Pays: England
ID NLM: 101222974

Informations de publication

Date de publication:
09 Jul 2019
Historique:
received: 27 11 2018
accepted: 11 06 2019
entrez: 11 7 2019
pubmed: 11 7 2019
medline: 14 1 2020
Statut: epublish

Résumé

Spinal cord injury (SCI) is a condition with few effective treatment options. The blood-spinal cord barrier consists of pericytes, astrocytes, and endothelial cells, which are collectively termed the neurovascular unit. These cells support spinal cord homeostasis by expressing tight junction proteins. Physical trauma to the spinal cord disrupts the barrier, which leads to neuroinflammation by facilitating immune cell migration to the damaged site in a process involving immune cell adhesion. Immunosuppressive strategies, including methylprednisolone (MPSS), have been investigated to treat SCI. However, despite some success, MPSS has the potential to increase a patient's susceptibility to wound infection and impaired wound healing. Hence, immunomodulation may be a more attractive approach than immunosuppression. Approved for modulating neuroinflammation in certain disorders, including Guillain-Barre syndrome, intravenous administration of human immunoglobulin G (hIgG) has shown promise in the setting of experimental SCI, though the optimal dose and mechanism of action remain undetermined. Female adult Wistar rats were subjected to moderate-severe clip compression injury (35 g) at the C7-T1 level and randomized to receive a single intravenous (IV) bolus of hIgG (0.02, 0.2, 0.4, 1, 2 g/kg), MPSS (0.03 g/kg), or control buffer at 15 min post-SCI. At 24 h and 6 weeks post-SCI, molecular, histological, and neurobehavioral effects of hIgG were analyzed. At 24 h post-injury, human immunoglobulin G co-localized with spinal cord pericytes, astrocytes, and vessels. hIgG (2 g/kg) protected the spinal cord neurovasculature after SCI by increasing tight junction protein expression and reducing inflammatory enzyme expression. Improvements in vascular integrity were associated with changes in spinal cord inflammation. Interestingly, hIgG (2 g/kg) increased serum expression of inflammatory cytokines and co-localized (without decreasing protein expression) with spinal cord vascular cell adhesion molecule-1, a protein used by immune cells to enter into inflamed tissue. Acute molecular benefits of hIgG (2 g/kg) led to greater tissue preservation, functional blood flow, and neurobehavioral recovery at 6 weeks post-SCI. Importantly, the effects of hIgG (2 g/kg) were superior to control buffer and hIgG (0.4 g/kg), and comparable with MPSS (0.03 g/kg). hIgG (2 g/kg) is a promising therapeutic approach to mitigate secondary pathology in SCI through antagonizing immune cell infiltration at the level of the neurovascular unit.

Sections du résumé

BACKGROUND BACKGROUND
Spinal cord injury (SCI) is a condition with few effective treatment options. The blood-spinal cord barrier consists of pericytes, astrocytes, and endothelial cells, which are collectively termed the neurovascular unit. These cells support spinal cord homeostasis by expressing tight junction proteins. Physical trauma to the spinal cord disrupts the barrier, which leads to neuroinflammation by facilitating immune cell migration to the damaged site in a process involving immune cell adhesion. Immunosuppressive strategies, including methylprednisolone (MPSS), have been investigated to treat SCI. However, despite some success, MPSS has the potential to increase a patient's susceptibility to wound infection and impaired wound healing. Hence, immunomodulation may be a more attractive approach than immunosuppression. Approved for modulating neuroinflammation in certain disorders, including Guillain-Barre syndrome, intravenous administration of human immunoglobulin G (hIgG) has shown promise in the setting of experimental SCI, though the optimal dose and mechanism of action remain undetermined.
METHODS METHODS
Female adult Wistar rats were subjected to moderate-severe clip compression injury (35 g) at the C7-T1 level and randomized to receive a single intravenous (IV) bolus of hIgG (0.02, 0.2, 0.4, 1, 2 g/kg), MPSS (0.03 g/kg), or control buffer at 15 min post-SCI. At 24 h and 6 weeks post-SCI, molecular, histological, and neurobehavioral effects of hIgG were analyzed.
RESULTS RESULTS
At 24 h post-injury, human immunoglobulin G co-localized with spinal cord pericytes, astrocytes, and vessels. hIgG (2 g/kg) protected the spinal cord neurovasculature after SCI by increasing tight junction protein expression and reducing inflammatory enzyme expression. Improvements in vascular integrity were associated with changes in spinal cord inflammation. Interestingly, hIgG (2 g/kg) increased serum expression of inflammatory cytokines and co-localized (without decreasing protein expression) with spinal cord vascular cell adhesion molecule-1, a protein used by immune cells to enter into inflamed tissue. Acute molecular benefits of hIgG (2 g/kg) led to greater tissue preservation, functional blood flow, and neurobehavioral recovery at 6 weeks post-SCI. Importantly, the effects of hIgG (2 g/kg) were superior to control buffer and hIgG (0.4 g/kg), and comparable with MPSS (0.03 g/kg).
CONCLUSIONS CONCLUSIONS
hIgG (2 g/kg) is a promising therapeutic approach to mitigate secondary pathology in SCI through antagonizing immune cell infiltration at the level of the neurovascular unit.

Identifiants

pubmed: 31288834
doi: 10.1186/s12974-019-1518-0
pii: 10.1186/s12974-019-1518-0
pmc: PMC6615094
doi:

Substances chimiques

Immunoglobulins, Intravenous 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

141

Subventions

Organisme : Baxter Healthcare Corporation
ID : N/A
Organisme : Gerald and Tootsie Halbert Chair in Neural Repair and Regeneration
ID : N/A
Organisme : Frederick Banting and Charles Best Graduate Scholarship (CIHR)
ID : N/A

Références

Exp Neurol. 1999 Aug;158(2):351-65
pubmed: 10415142
Neuroreport. 2000 Nov 9;11(16):3551-4
pubmed: 11095516
J Neurosci. 2002 Sep 1;22(17):7526-35
pubmed: 12196576
Immunology. 2002 Dec;107(4):387-93
pubmed: 12460182
Neurology. 2002 Dec 24;59(12 Suppl 6):S13-21
pubmed: 12499466
Blood. 2003 Jul 15;102(2):558-60
pubmed: 12649142
J Comp Neurol. 2003 Jul 21;462(2):223-40
pubmed: 12794745
J Neurochem. 2004 Mar;88(6):1335-44
pubmed: 15009633
Neuroscience. 2004;124(4):945-52
pubmed: 15026134
J Neurosci. 2004 Apr 21;24(16):4043-51
pubmed: 15102919
J Neurosurg Anesthesiol. 2005 Apr;17(2):82-5
pubmed: 15840993
Circulation. 2005 Sep 27;112(13):2031-9
pubmed: 16172269
J Neurotrauma. 2006 Mar-Apr;23(3-4):318-34
pubmed: 16629619
J Neurosurg Spine. 2006 Oct;5(4):343-52
pubmed: 17048772
Eur J Neurosci. 2007 Mar;25(6):1743-7
pubmed: 17432962
Acta Med Okayama. 2007 Apr;61(2):89-98
pubmed: 17471309
Exp Neurol. 2008 Feb;209(2):378-88
pubmed: 17662717
Brain Res. 2008 Jan 16;1189:1-11
pubmed: 18061148
Annu Rev Immunol. 2008;26:513-33
pubmed: 18370923
Neuroscience. 2009 Feb 6;158(3):1194-9
pubmed: 18790013
J Neurosci. 2009 Jan 21;29(3):753-64
pubmed: 19158301
J Neurochem. 2009 Mar;108(6):1360-72
pubmed: 19183262
J Clin Neurosci. 2009 Apr;16(4):549-53
pubmed: 19200733
Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4788-92
pubmed: 19261857
Pediatr Allergy Immunol. 2009 May;20(3):266-72
pubmed: 19438983
J Neurochem. 2009 Sep;110(5):1547-56
pubmed: 19627440
Science. 2009 Jul 31;325(5940):612-6
pubmed: 19644120
Clin Exp Immunol. 2009 Dec;158 Suppl 1:2-13
pubmed: 19883419
J Neurosci Res. 2010 Jun;88(8):1615-31
pubmed: 20127816
Autoimmunity. 2010 Dec;43(8):619-27
pubmed: 20380586
Nature. 2010 Nov 25;468(7323):557-61
pubmed: 20944627
J Biol Chem. 2011 Jan 21;286(3):2308-19
pubmed: 21071446
J Allergy Clin Immunol. 2011 Feb;127(2):315-23; quiz 324-5
pubmed: 21185071
Brain. 2011 Mar;134(Pt 3):704-20
pubmed: 21354973
Science. 2011 Jul 8;333(6039):238-42
pubmed: 21737741
Exp Neurol. 2011 Oct;231(2):272-83
pubmed: 21784069
J Neuroinflammation. 2011 Aug 26;8:106
pubmed: 21867555
Clin Immunol. 2011 Nov;141(2):187-96
pubmed: 21917526
J Neurotrauma. 2012 May 20;29(8):1626-37
pubmed: 22150233
Eur J Immunol. 2012 Aug;42(8):2121-31
pubmed: 22585560
J Neuroinflammation. 2012 Sep 21;9:224
pubmed: 22998664
J Dermatol Sci. 2013 Jan;69(1):77-80
pubmed: 23102713
Toxicol Ind Health. 2014 Oct;30(9):851-60
pubmed: 23104729
Crit Rev Biochem Mol Biol. 2013 May-Jun;48(3):222-72
pubmed: 23547785
J Neurotrauma. 2013 Aug 1;30(15):1311-24
pubmed: 23731227
J Neurosci. 2013 Aug 7;33(32):12970-81
pubmed: 23926252
J Cereb Blood Flow Metab. 2013 Dec;33(12):1983-92
pubmed: 24045402
J Allergy Clin Immunol. 2014 Mar;133(3):853-63.e5
pubmed: 24210883
J Neurotrauma. 2014 Mar 15;31(6):541-52
pubmed: 24237182
J Immunol. 2014 Jan 15;192(2):792-803
pubmed: 24342805
J Clin Immunol. 2014 Jul;34 Suppl 1:S132-8
pubmed: 24722853
J Neurotrauma. 2014 Nov 1;31(21):1767-75
pubmed: 24831774
Front Cell Neurosci. 2014 May 13;8:129
pubmed: 24860431
J Neurotrauma. 2014 Nov 1;31(21):1753-66
pubmed: 24934600
Neuropharmacology. 2014 Oct;85:408-16
pubmed: 24937047
Stem Cells Transl Med. 2014 Oct;3(10):1148-59
pubmed: 25107585
Acta Neuropathol. 2015 Feb;129(2):259-77
pubmed: 25391494
Front Immunol. 2015 Apr 28;6:197
pubmed: 25972869
J Control Release. 2015 Dec 10;219:141-154
pubmed: 26343846
Brain. 2016 Mar;139(Pt 3):692-707
pubmed: 26754788
J Clin Immunol. 2016 May;36 Suppl 1:83-7
pubmed: 26957094
Nat Neurosci. 2016 Jun;19(6):784-7
pubmed: 27089020
Exp Neurol. 2016 Sep;283(Pt B):550-9
pubmed: 27151600
Stem Cells Transl Med. 2016 Aug;5(8):991-1003
pubmed: 27245367
Ann Clin Transl Neurol. 2016 May 25;3(7):495-511
pubmed: 27386499
Dis Model Mech. 2016 Oct 1;9(10):1125-1137
pubmed: 27736748
J Neurotrauma. 2017 Mar 15;34(6):1209-1226
pubmed: 27775474
Sci Rep. 2017 Jan 11;7:40528
pubmed: 28074934
Am J Transl Res. 2017 Mar 15;9(3):1012-1024
pubmed: 28386329
Front Immunol. 2018 Jun 08;9:1299
pubmed: 29951056
J Neurotrauma. 2019 Apr 24;:null
pubmed: 30843463
Exp Neurol. 1995 Apr;132(2):220-8
pubmed: 7789460
J Neurosurg. 1977 Oct;47(4):577-81
pubmed: 903810
JAMA. 1997 May 28;277(20):1597-604
pubmed: 9168289
Neuroscience. 1997 Aug;79(4):1177-82
pubmed: 9219976

Auteurs

Jonathon Chon Teng Chio (JCT)

Department of Genetics and Development, Krembil Research Institute, University Health Network, Krembil Discovery Tower, 60 Leonard Avenue, 7KD-430, Toronto, Ontario, M5T 2S8, Canada.
Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada.
Spinal Program, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada.

Jian Wang (J)

Department of Genetics and Development, Krembil Research Institute, University Health Network, Krembil Discovery Tower, 60 Leonard Avenue, 7KD-430, Toronto, Ontario, M5T 2S8, Canada.

Anna Badner (A)

Sue and Bill Gross Stem Cell Research Centre, University of California, 845 Health Sciences Road, Irvine, CA, 92617, USA.

James Hong (J)

Department of Genetics and Development, Krembil Research Institute, University Health Network, Krembil Discovery Tower, 60 Leonard Avenue, 7KD-430, Toronto, Ontario, M5T 2S8, Canada.
Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada.
Spinal Program, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada.

Vithushan Surendran (V)

University of Toronto, Toronto, Ontario, Canada.

Michael G Fehlings (MG)

Department of Genetics and Development, Krembil Research Institute, University Health Network, Krembil Discovery Tower, 60 Leonard Avenue, 7KD-430, Toronto, Ontario, M5T 2S8, Canada. michael.fehlings@uhn.ca.
Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada. michael.fehlings@uhn.ca.
Spinal Program, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada. michael.fehlings@uhn.ca.
University of Toronto, Toronto, Ontario, Canada. michael.fehlings@uhn.ca.
Gerry and Tootsie Halbert Chair in Neural Repair and Regeneration, University of Toronto, Toronto, Canada. michael.fehlings@uhn.ca.
Krembil Neuroscience Program, Toronto Western Hospital, University Health Network, 399 Bathurst Street, Toronto, Ontario, M5T 2S8, Canada. michael.fehlings@uhn.ca.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH