The Spleen Plays No Role in Nephrotoxic Serum Nephritis, but Constitutes a Place of Compensatory Haematopoiesis

PLoS One. 2015 Aug 6;10(8):e0135087. doi: 10.1371/journal.pone.0135087. eCollection 2015.

Abstract

Background: The spleen has been implicated in the pathogenesis of immune-complex glomerulonephritis by initiating and resolving adaptive immune responses. Thus, we aimed to evaluate the role of the spleen in experimental nephrotoxic serum nephritis (NTS).

Methods: In order to accelerate the disease, animals were subjected to NTS by preimmunizing male C57BL/6J mice with rabbit IgG three days before injecting the rabbit anti-glomerular basement antiserum, or were immunized only. A group underwent splenectomy before NTS induction.

Results: We observed enlargement of the spleen with a maximum at 14 days after NTS induction or immunization only. Splenectomized mice were found to develop albuminuria and renal histological changes comparable to sham-operated controls. Nevertheless, anaemia was aggravated in mice after splenectomy. During the course of NTS, we detected CD41+ megakaryocytes and Ter119+ erythroid precursor cells in the spleen of mice with NTS and of immunized mice. Ter119+Cxcr4+ cells and the binding partner Cxcl12 increased in the spleen, and decreased in the bone marrow. This was accompanied by a significant systemic increase of interferon-gamma in the serum.

Conclusions: In summary, splenectomy does not influence the course of NTS per se, but is involved in concomitant anaemia. Extramedullary haematopoiesis in the spleen is probably facilitated through the migration of Cxcr4+ erythroid precursor cells from the bone marrow to the spleen via a Cxcl12 gradient and likely arises from the suppressive capacity of chronic inflammation on the bone marrow.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Albuminuria / etiology
  • Albuminuria / genetics
  • Albuminuria / immunology
  • Albuminuria / pathology
  • Anemia / etiology
  • Anemia / genetics
  • Anemia / immunology
  • Anemia / pathology
  • Animals
  • Blood Group Antigens / genetics
  • Blood Group Antigens / immunology
  • Bone Marrow / immunology
  • Bone Marrow / pathology
  • Chemokine CXCL12 / genetics
  • Chemokine CXCL12 / immunology
  • Gene Expression
  • Hematopoiesis, Extramedullary / immunology*
  • Immune Sera / adverse effects
  • Immunization
  • Immunoglobulin G / adverse effects
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Kidney Glomerulus / immunology
  • Kidney Glomerulus / pathology
  • Male
  • Megakaryocytes / immunology
  • Megakaryocytes / pathology
  • Mice
  • Mice, Inbred C57BL
  • Nephritis / chemically induced
  • Nephritis / genetics
  • Nephritis / immunology
  • Nephritis / pathology*
  • Nephrotic Syndrome / chemically induced
  • Nephrotic Syndrome / genetics
  • Nephrotic Syndrome / immunology
  • Nephrotic Syndrome / pathology*
  • Rabbits
  • Receptors, CXCR4 / genetics
  • Receptors, CXCR4 / immunology
  • Spleen / immunology*
  • Spleen / pathology
  • Splenectomy / adverse effects*

Substances

  • Blood Group Antigens
  • CXCR4 protein, mouse
  • Chemokine CXCL12
  • Cxcl12 protein, mouse
  • Immune Sera
  • Immunoglobulin G
  • Receptors, CXCR4
  • TER-119 antigen, mouse
  • Interferon-gamma