Negative feedback on the effects of stem cell factor on hematopoiesis is partly mediated through neutral endopeptidase activity on substance P: a combined functional and proteomic study

Blood. 2001 Nov 1;98(9):2697-706. doi: 10.1182/blood.v98.9.2697.

Abstract

Hematopoietic regulation is a complex but dynamic process regulated by intercellular and intracellular interactions within the bone marrow (BM) microenvironment. Through neurokinin-1 (NK-1) and NK-2 receptors, peptides (eg, substance P [SP]) encoded by the preprotachykinin-I gene mediate distinct hematopoietic effects. Cytokines, associated with hematopoietic stimulation, and SP regulate the expression of each other in BM mesenchymal and immune cells. Neutral endopeptidase (NEP) uses SP as a substrate to produce SP(1-4), which inhibits the proliferation of matured myeloid progenitor. This study determines whether the degradation of SP to SP(1-4) by endogenous NEP in BM stroma could be a feedback on hematopoietic stimulation by stem cell factor (SCF). SP(1-4) induced the production of transforming growth factor (TGF)-beta and tumor necrosis factor-alpha in BM stroma. TGF-beta production accounted for part of the inhibitory effects by SP(1-4) on the proliferation of early (granulocyte-macrophage colony-forming units) and late (long-term culture-initiating cells) hematopoietic progenitors. Enzyme-linked immunosorbent assays and/or protein-chip arrays indicated a timeline change of SP to SP(1-4) in BM stroma stimulated with SCF, which correlated with increase in NEP messenger RNA. Since SP and its fragment, SP(1-4), interact with the same receptor to mediate opposing hematopoietic effects, 2 interactive studies were done to understand the dual responses of NK-1: (1) a 3-dimensional molecular model of NK-1 and SP and (2) screening of a random dodecapeptide library for SP(1-4) interacting sites. The effects of SP(1-4) on hematopoietic progenitors and the timeline change of SP to SP(1-4), together with the 3-dimensional model, provide a partial explanation for the feedback on the stimulatory effects of SCF and SP on hematopoiesis.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Binding Sites
  • Bone Marrow Cells
  • Discoidin Domain Receptor 1
  • Feedback, Physiological*
  • Hematopoiesis / drug effects*
  • Hematopoietic Stem Cells / drug effects
  • Humans
  • Membrane Proteins
  • Models, Molecular
  • Neprilysin / metabolism*
  • Neprilysin / pharmacology
  • Peptide Library
  • RNA, Messenger / drug effects
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptors, Neurokinin-1 / drug effects
  • Receptors, Neurokinin-1 / metabolism
  • Receptors, Neurokinin-2 / drug effects
  • Receptors, Neurokinin-2 / metabolism
  • Stem Cell Factor / pharmacology*
  • Stem Cell Factor / physiology
  • Substance P / metabolism*
  • Substance P / pharmacology
  • Substance P / physiology
  • Transforming Growth Factor beta / drug effects
  • Transforming Growth Factor beta / metabolism
  • Tumor Necrosis Factor-alpha / drug effects
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Membrane Proteins
  • Peptide Library
  • RNA, Messenger
  • Receptors, Neurokinin-1
  • Receptors, Neurokinin-2
  • Stem Cell Factor
  • Transforming Growth Factor beta
  • Tumor Necrosis Factor-alpha
  • Substance P
  • Ddr1 protein, mouse
  • Discoidin Domain Receptor 1
  • Receptor Protein-Tyrosine Kinases
  • Neprilysin