Long‐Term Multilayer Adherent Network (MAN) Expansion, Maintenance, and Characterization, Chemical and Genetic Manipulation, and Transplantation of Human Fetal Forebrain Neural Stem Cells

Dustin R. Wakeman1, Martin R. Hofmann1, D. Eugene Redmond2, Yang D. Teng3, Evan Y. Snyder1

1 The Burnham Institute for Medical Research, La Jolla, California, 2 Yale University School of Medicine, New Haven, Connecticut, 3 Veterans Affairs Boston Healthcare System, Boston, Massachusetts
Publication Name:  Current Protocols in Stem Cell Biology
Unit Number:  Unit 2D.3
DOI:  10.1002/9780470151808.sc02d03s9
Online Posting Date:  May, 2009
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Abstract

Human neural stem/precursor cells (hNSC/hNPC) have been targeted for application in a variety of research models and as prospective candidates for cell‐based therapeutic modalities in central nervous system (CNS) disorders. To this end, the successful derivation, expansion, and sustained maintenance of undifferentiated hNSC/hNPC in vitro, as artificial expandable neurogenic micro‐niches, promises a diversity of applications as well as future potential for a variety of experimental paradigms modeling early human neurogenesis, neuronal migration, and neurogenetic disorders, and could also serve as a platform for small‐molecule drug screening in the CNS. Furthermore, hNPC transplants provide an alternative substrate for cellular regeneration and restoration of damaged tissue in neurodegenerative disorders such as Parkinson's disease and Alzheimer's disease. Human somatic neural stem/progenitor cells (NSC/NPC) have been derived from a variety of cadaveric sources and proven engraftable in a cytoarchitecturally appropriate manner into the developing and adult rodent and monkey brain while maintaining both functional and migratory capabilities in pathological models of disease. In the following unit, we describe a new procedure that we have successfully employed to maintain operationally defined human somatic NSC/NPC from developing fetal, pre‐term post‐natal, and adult cadaveric forebrain. Specifically, we outline the detailed methodology for in vitro expansion, long‐term maintenance, manipulation, and transplantation of these multipotent precursors. Curr. Protoc. Stem Cell Biol. 9:2D.3.1‐2D.3.77. © 2009 by John Wiley & Sons, Inc.

Keywords: human neural stem/progenitor cell; NPC; NSC; culture; fetal/adult forebrain; subventricular zone; neurogenesis; niche; multilayer adherent network; MAN assay; protocols; manipulation techniques; characterization; in vitro; derivation; expansion; maintenance; SPIO; Feridex; lentivirus; BrdU; labeling

     
 
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Table of Contents

  • Introduction
  • Strategic Planning
  • Long‐Term Expansion and Maintenance of hNPC
  • Basic Protocol 1: Establishing and Maintaining Multilayer Adherent Network (MAN) Cultures
  • Support Protocol 1: Derivation of Human Fetal Neural Stem/Precursor Cells
  • Alternate Protocol 1: Feeding and Dissociation of Lightly Adherent Aggregate Cultures
  • Alternate Protocol 2: Growing hNPC in MAN Membrane System (MMS)
  • Support Protocol 2: Cryopreservation of hNPC
  • Support Protocol 3: Thawing Cryopreserved hNPC
  • Support Protocol 4: Preservation of Conditioned Medium
  • Alternate Protocol 3: Replating Dissociated hNSC on Extracellular Matrix (ECM) as Adherent Two‐Dimensional Monolayer Cultures
  • Support Protocol 5: Preparation of Extracellular Matrix (ECM) Substrates
  • Basic Protocol 2: Establishing Clonal hNPC Subpopulations
  • Labeling hNPC Pre‐Transplantation
  • Basic Protocol 3: Labeling hNPC with BrdU
  • Basic Protocol 4: Lentiviral Infection of hNPC
  • Alternate Protocol 4: Lentiviral Infection of Multilayer Adherent Network (MAN)
  • Basic Protocol 5: Labeling hNPC with Super‐Paramagnetic Iron Oxide (SPIO)
  • Support Protocol 6: Perls Prussian Blue Staining (for Hemosiderin)
  • Basic Protocol 6: Preparing hNPC for Transplantation
  • Basic Protocol 7: Loading and Injection of hNPC for Transplantation into St. Kitts African Green Monkey
  • Basic Protocol 8: Intraventricular Injection of hNPC into Neonatal Mice
  • Basic Protocol 9: Processing Engrafted Mouse Brains
  • Basic Protocol 10: Characterizing hNPC
  • Reagents and Solutions
  • Commentary
  • Literature Cited
  • Figures
  • Tables
     
 
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Materials

Basic Protocol 1: Establishing and Maintaining Multilayer Adherent Network (MAN) Cultures

  Materials
  • Human NPC ( protocol 2): frozen ( protocol 5) and freshly thawed ( protocol 6) or freshly dissociated as described in protocol 2
  • 25% (v/v) conditioned medium (CM; protocol 7)/75% (v/v) NB‐B‐27 complete medium (see recipe) containing 40 ng/ml bFGF and 10 ng/ml LIF (bFGF and LIF concentrations based on total volume of medium)
  • NB‐B‐27 complete medium (see recipe)
  • Leukemia inhibitor factor (LIF; Millipore, cat. no. LIF1010)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • Dulbecco's PBS without Ca2+ or Mg2+ (CMF‐DPBS; Mediatech, cat. no. 21‐031‐CM)
  • Accutase (Millipore, cat. no. SCR005) or Cell Dissociation Buffer (Invitrogen, cat. no. 13150‐016)
  • Conditioned medium (CM; protocol 7)
  • 15‐ml conical tubes
  • 25‐cm2 and 75‐cm2 tissue culture flasks
  • Battery‐powered pipetting aid (e.g., Drummond Pipet‐Aid XP)
  • 1000‐µl extended‐length pipet tip and 1000‐µl automatic pipettor
  • Centrifuge
  • Additional reagents and equipment for counting viable cells by trypan blue exclusion (unit 1.3)

Support Protocol 1: Derivation of Human Fetal Neural Stem/Precursor Cells

  Materials
  • Fetal tissue
  • 10% (v/v) formalin (optional)
  • Enzymes for tissue dissociation (optional): e.g., Accutase, trypsin‐EDTA, PPD (papain‐protease‐DNase I)
  • Fetal bovine serum (FBS; optional)
  • NB‐B‐27 complete medium (see recipe)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • Leukemia inhibitory factor (LIF; Millipore, cat. no. LIF1010)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Epidermal growth factor (EGF; Millipore, cat. no. 01‐107)
  • Surgical equipment, including scalpel, sterile
  • 15‐ml conical tubes
  • Battery‐powered pipetting aid (e.g., Drummond Pipet‐Aid XP)
  • Additional reagents and equipment for counting viable cells by trypan blue exclusion (unit 1.3)

Alternate Protocol 1: Feeding and Dissociation of Lightly Adherent Aggregate Cultures

  Materials
  • Human NPC growing in 25‐cm2 flasks ( protocol 2)
  • NB‐B27 complete medium (see recipe)
  • Accutase (Millipore, cat. no. SCR005) or Cell Dissociation Buffer (Invitrogen, cat. no. 13150‐016)
  • Battery‐powered pipetting aid (e.g., Drummond Pipet‐Aid XP)
  • 15‐ml conical tubes
  • Centrifuge
  • Pipettors with extended‐length pipet tips

Alternate Protocol 2: Growing hNPC in MAN Membrane System (MMS)

  Materials
  • NB‐B‐27 complete medium (see recipe)
  • Leukemia inhibitor factor (LIF; Millipore, cat. no. LIF1010)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Freshly dissociated hNPC or small aggregates ( protocol 2)
  • 6‐well tissue culture plates
  • Forceps, sterile
  • 1.0 to 0.1‐µm hanging basket transmembrane cell culture insert (Corning)

Support Protocol 2: Cryopreservation of hNPC

  Materials
  • 70% ethanol
  • Cultures of hNPC grown in 25‐cm2 flasks dissociated 48 to 72 hr earlier ( protocol 2)
  • NB‐B‐27 complete medium (see recipe)
  • hNPC freezing medium (see recipe)
  • Liquid N 2
  • 1.8‐ml cryovials (Nunc, cat. no. 377267) and labels
  • 15‐ and 50‐ml conical tubes
  • Battery‐powered pipetting aid (e.g., Drummond Pipet‐Aid XP)
  • Controlled‐rate freezing device (e.g., “Mr. Frosty”; Nalgene)
  • Liquid N 2 tank

Support Protocol 3: Thawing Cryopreserved hNPC

  Materials
  • Frozen hNPC in 1.8‐ml cryovials ( protocol 6)
  • 70% ethanol
  • Thaw medium: 50% (v/v) conditioned medium ( protocol 7)/50% (v/v) NB‐B‐27 complete medium (see recipe)
  • Thaw medium (see above) containing 10 ng/ml leukemia inhibitory factor (LIF; Millipore, cat. no. LIF1010) and 20 ng/ml basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • 15‐ml conical tubes
  • 25‐cm2 tissue culture flasks (non‐ECM‐coated)

Support Protocol 4: Preservation of Conditioned Medium

  Materials
  • Human NPC MAN culture, 65% to 75% confluent ( protocol 1) in 25‐cm2 flask
  • NB‐B‐27 complete medium (see recipe)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • Leukemia inhibitory factor (LIF; Millipore, cat. no. LIF1010)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Acrodisc sterile syringe filter (0.2‐µm; Pall, cat. no. 4433)
  • 15‐ml conical tubes

Alternate Protocol 3: Replating Dissociated hNSC on Extracellular Matrix (ECM) as Adherent Two‐Dimensional Monolayer Cultures

  Materials
  • 100% ethanol
  • Poly‐D‐lysine hydrobromide (Sigma, cat. no. P6407) or poly‐L‐ornithine (Sigma, cat. no. P4957)
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • 0.1% (w/v) fibronectin from human plasma (Sigma, cat. no. F0895)
  • Laminin, human (0.5 mg/ml; Sigma, cat. no. L6274) or murine (Sigma, cat. no. L2020)
  • Matrigel, growth factor–reduced (BD Bioscience, cat. no. 354230)
  • Neurobasal medium (Invitrogen, cat. no. 21103049), cold
  • Glass coverslips (Fisher, cat. no. NC970884)
  • 24‐well tissue culture plates
  • Forceps, sterile
  • 15‐ml conical tubes
  • Ziploc bag

Support Protocol 5: Preparation of Extracellular Matrix (ECM) Substrates

  Materials
  • Human NPC ( protocol 1 or protocol 2)
  • NB‐B‐27 complete medium (see recipe)
  • Conditioned medium (CM; protocol 7)
  • Leukemia inhibitor factor (LIF; Millipore, cat. no. LIF1010)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Complete Hibernate‐E medium (see recipe)
  • 15‐ml conical tubes
  • Fluorescence activated cell sorting (FACS) machine (Robinson et al., )
  • 96‐well plates
  • Additional reagents and equipment for dissociating hNPC ( protocol 1 or protocol 3) and flow cytometry (Robinson et al., )

Basic Protocol 2: Establishing Clonal hNPC Subpopulations

  Materials
  • NB‐B‐27 complete medium (see recipe)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Leukemia inhibitor factor (LIF; Millipore, cat. no. LIF1010)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • 5‐bromo‐2′‐deoxyuridine (BrdU; Sigma, cat. no. 59‐14‐3; see recipe)
  • 25‐cm2 tissue culture flasks

Basic Protocol 3: Labeling hNPC with BrdU

  Materials
  • Human NPC, single cells or lightly adherent aggregates ( protocol 1 or protocol 3)
  • NB‐B‐27 complete medium (see recipe)
  • Normocin (InvivoGEN, cat. no. ant‐nr‐1)
  • Leukemia inhibitor factor (LIF; Millipore, cat. no. LIF1010)
  • Basic fibroblast growth factor (bFGF; Millipore, cat. no. GF003)
  • 10 mg/ml polybrene (Chemicon)
  • Lentivirus (see protocol introduction for information)
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • 25‐cm2 tissue culture flasks
  • 15‐ml conical tubes

Basic Protocol 4: Lentiviral Infection of hNPC

  • 60% to 80% confluent (2 to 3 weeks in vitro) MAN hNPC culture in 25‐cm2 flask ( protocol 1) or in transmembrane basket
  • 6‐well tissue culture plates
  • Hanging Basket Cell Culture Insert, 1.0 µm (Millipore, cat. no. PIRP30R48)
  • 25‐cm2 tissue culture flasks

Alternate Protocol 4: Lentiviral Infection of Multilayer Adherent Network (MAN)

  • Human NPC ( protocol 1 or protocol 3)
  • Feridex (Bayer Healthcare Pharmaceuticals, cat. no. NDC‐59338‐7035‐5)
  • Protamine sulfate injection, USP, 50 mg/5 ml (Bayer Healthcare Pharmaceuticals, cat no. NDC‐63323‐229‐05)
  • 25‐cm2 tissue culture flasks
  • 15‐ml conical tubes
  • Centrifuge

Basic Protocol 5: Labeling hNPC with Super‐Paramagnetic Iron Oxide (SPIO)

  Materials
  • Potassium ferrocyanide
  • HCl, concentrated
  • Sample: SPIO‐labeled hNPC ( protocol 14) or cardiac‐perfused ( protocol 18) tissue sections from transplanted animals ( protocol 17 or protocol 188)
  • Fixative: e.g., 4% paraformaldehyde (PFA; see recipe) or equivalent
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • Nuclear counterstain, e.g., neutral red, DAPI, propidium iodide

Support Protocol 6: Perls Prussian Blue Staining (for Hemosiderin)

  Materials
  • Human NPC (hNPC): small to medium aggregate clusters ( protocol 1 or protocol 3)
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • 0.4% (v/v) trypan blue
  • Hemacytometer (unit 1.3)
  • Additional reagents and equipment for counting viable cells using a hemacytometer and trypan blue (unit 1.3)

Basic Protocol 6: Preparing hNPC for Transplantation

  Materials
  • Experimental animals: St. Kitts African Green Monkey (MPTP‐treated or PBS sham control)
  • Ketamine hydrochloride injection, USP (Ketaset, Fort Dodge Animal Health)
  • Atropine for i.m. or s.c. administration
  • Pentobarbital for i.v. administration
  • Lubrivet (optional; Butler Animal Health; http://www.accessbutler.com/)
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • 70% ethanol
  • Human NPC (hNPC; protocol 16), labeled according to any of the pretransplantation labeling procedures described in this unit
  • NB‐B‐27 complete medium (see recipe) without Normocin
  • Phosphate‐buffered saline (PBS)
  • 100‐µl syringe (Hamilton) for stereotactic injection
  • 22‐G, 2‐in. needle (Hamilton) for stereotactic injection
  • Single syringe microinjectors for Hamilton syringes (Stoelting)
  • Primate or large animal size stereotaxic head holder and bars (David Kopf Instruments)
  • Ear bars (David Kopf Instruments)
  • Animal clippers
  • Endotracheal tube
  • Sterile surgical supplies including:
    • Stereotactic bone drill with 0.5‐mm drill burrs
    • Drapes
    • Forceps
    • Hemostats
    • Needle holders
    • Periostial elevators
    • Scalpel with no. 10 surgical blade (Bard–Parker)
    • Self‐retaining retractor
    • Towel clips
    • Standard neurosurgical supplies—sutures, bone wax, Gelfoam, sterile NaCl irrigation solution
    • 3‐in. sterile gauze
  • EKG machine with monitoring leads
  • Leads for temperature and O 2 saturation
  • Additional reagents and equipment for counting viable cells with a hemacytometer and trypan blue (unit 1.3)

Basic Protocol 7: Loading and Injection of hNPC for Transplantation into St. Kitts African Green Monkey

  Materials
  • Neonatal mice (P0 to P3) of appropriate strain
  • 70% ethanol
  • Dulbecco's PBS with Ca2+ and Mg2+ (DPBS; Mediatech, cat. no. 21‐030‐CM)
  • Human NPC (hNPC; protocol 16; 50,000 cells/µl) in microcentrifuge tube
  • Borosilicate glass (Sutter Instrument Co., cat. no. B100–75‐15)
  • Micropipet puller (Sutter Instrument Co., Model P‐87)
  • Aspirator tube assemblies for calibrated microcapillary pipets (Sigma Aldrich, cat. no.A5177–5EA)
  • Fiber optic light source for transillumination (Dolan‐Jenner Industries)
  • Warm‐water glove balloon
  • Additional reagents and equipment for preparing injection micropipet (Lee et al., ) and processing mouse brains ( protocol 19)

Basic Protocol 8: Intraventricular Injection of hNPC into Neonatal Mice

  Materials
  • Injected experimental animals ( protocol 18)
  • Anesthetic: Isoflurane or pentobarbital
  • Dulbecco's PBS without Ca2+ or Mg2+ (CMF‐DPBS; Mediatech, cat. no. 21‐031‐CM)
  • 4% paraformaldehyde (PFA; see recipe), cold
  • 10% and 30% (w/v) sucrose in PBS
  • OCT embedding medium (e.g., Fisher)
  • Dry ice
  • 2‐methylbutane (Fisher, cat. no. 03551‐4)
  • Sodium azide
  • Low‐melt agarose (UltraPure Low Melting Point Agarose; Invitrogen, cat. no. 16520050)
  • Dissection tools: scalpel, fine scissors, forceps, spatula, and pins
  • Perfusion Apparatus: pump and leads
  • Appropriate embedding mold
  • Charged slides (Fisher Superfrost Plus)
  • Cryostat microtome or vibratome
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Literature Cited

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