Tracking Superparamagnetic Iron Oxide
Labeled Monocytes in Brain by High-Field
Magnetic Resonance Imaging
Marina L. Zelivyanskaya,
1,2
Jay A. Nelson,
1,3
Larissa Poluektova,
1,2
Mariano Uberti,
1,5
Melissa Mellon,
1,3
Howard E. Gendelman,
1,2,4
*
and Michael D. Boska
1,3
1
Center for Neurovirology and Neurodegenerative Disorders, University of Nebraska Medical Center,
Omaha, Nebraska
2
Department of Pathology & Microbiology, University of Nebraska Medical Center, Omaha, Nebraska
3
Department of Radiology, University of Nebraska Medical Center, Omaha, Nebraska
4
Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska
5
Department of Computer Science, PKI 170, University of Nebraska at Omaha, Omaha, Nebraska
Inflammatory cells, most notably mononuclear phago-
cytes (MP; macrophages and microglia), play a critical
role in brain homeostasis, repair and disease. One im-
portant event in cellular biodynamics is how MP move in
and throughout the nervous system. Prior studies have
focused principally on cell migration across the blood–
brain barrier during neuroinflammatory processes with
little work done on cell movement within the brain. During
the past decade our laboratories have studied the role of
MP in HIV-1-associated dementia (HAD). In HAD MP
incite sustained glial inflammatory reactions causing sig-
nificant neuronal damage. To extend these works we
investigated cell movement in brain and its influence for
disease in a novel co-registration system integrating neu-
ropathology with high-field magnetic resonance imaging
(MRI). Human monocytes labeled with superparamag-
netic iron oxide particles were injected into the brain of
severe combined immunodeficient (SCID) mice. MRI was
recorded 1, 7, and 14 days after cell injection. MRI co-
registered with histology verified that the MRI signal
modification was due to the labeled cells. MRI showed
human monocyte-derived macrophages along the injec-
tion site, the corpus callosum, the ventricular system and
in other brain sites. These data support the idea that cell
migration can be monitored in vivo and provides an
opportunity to assess monocyte mobility in brain and its
affects on neurodegenerative processes and notably
HAD. © 2003 Wiley-Liss, Inc.
Key Words: monocyte-derived macrophages; Feridex;
magnetic resonance imaging; histology MRI co-registra-
tion; SCID mice; HIV-1-associated dementia
Inflammatory cell trans migration is a critical com-
ponent of the disease process for many neurodegenerative
disorders (for example, Alzheimer’s and Parkinson’s dis-
ease [AD and PD] and HIV-1-associated dementia
[HAD]) (Gendelman, 1997; Al-Omaishi et al., 1999; Cot-
ter et al., 1999b; Swindells et al., 1999; Diesing et al.,
2002). Prior works have investigated cell migration across
the blood– brain barrier with little known about leukocyte
migration within the brain itself (Persidsky et al., 2000).
During the past two decades, our laboratories have
worked toward a better understanding of the role that
mononuclear phagocytes (MP; circulating monocytes,
monocyte-derived macrophages [MDM] and microglia)
play in HIV-1-associated dementia (HAD) as well as in
other lentiviral encephalopathies (Zink, 2002). It has been
demonstrated that virus-infected immune activated MP
directly affect the neurodegenerative disease process
(McArthur et al., 1992; Glass et al., 1995; Williams et al.,
2001; Gendelman, 2002). HAD, a late complication of
HIV-1 infection, is an example of how immune compe-
tent brain MP can affect neuronal and cognitive function.
HAD is characterized by severe cognitive, motor or be-
havior abnormalities (Navia et al., 1986a; McArthur et al.,
1999). Pathologically, HAD is linked to an encephalitis
where the infiltration, viral infection and immune activa-
tion of infected MP (Navia et al., 1986b; Glass et al., 1993)
and multinucleated giant cells abound (Sharer et al., 1985;
Budka, 1986). MP are the principal productively infected
cell in brain during disease (Gartner et al., 1986; Koenig et
al., 1986; Wiley et al., 1986).
It is accepted that macrophage secretory products
may lead to neuronal death during HAD. These include
pro-inflammatory cytokines, arachidonic acid and its me-
tabolites, platelet activating factor, quinolinic acid, matrix
Contract grant sponsor: National Institute of Health; Contract grant num-
ber: R37NS 36126, PO1 NS31492, and P01AI050244.
*Correspondence to: Howard E. Gendelman, MD, Center for Neurovi-
rology and Neurodegenerative Disorders, University of Nebraska Medical
Center, Omaha, NE 68198-5215. E-mail: hegendel@unmc.edu
Received 6 February 2003; Accepted 24 March 2003
Journal of Neuroscience Research 73:284 –295 (2003)
© 2003 Wiley-Liss, Inc.